Moving towards a new generation of animal models for asthma and COPD with improved clinical relevance

Pharmacology and Therapeutics

Volumn 130, Issue 2, 2011, Pages 93-105

  Stevenson, Christopher S ^a,b   Birrell, Mark A ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b Inflammation Discovery   (United States)

Author keywords

Acute exacerbation; Airway inflammation; Airway remodeling; Asthma; COPD; Emphysema

Indexed keywords

ALLERGEN; BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; CIGARETTE SMOKE; CYTOKINE; ELASTASE; GLUCOCORTICOID; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HOUSE DUST ALLERGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; MUSCARINIC RECEPTOR BLOCKING AGENT; OVALBUMIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ALLERGIC ASTHMA; ANTIINFLAMMATORY ACTIVITY; ASTHMA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYTOKINE PRODUCTION; DERMATOPHAGOIDES; DISEASE EXACERBATION; DISEASE PREDISPOSITION; DRUG EFFICACY; DRUG MEGADOSE; EOSINOPHIL; EXPERIMENTAL MODEL; HAEMOPHILUS INFLUENZAE; IN VIVO STUDY; LUNG INJURY; MORAXELLA CATARRHALIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RHINOVIRUS; SEVERE PERSISTENT ASTHMA; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ASTHMA; DISEASE MODELS, ANIMAL; HUMANS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE;

EID: 79953663682     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2010.10.008     Document Type: Review

References (176)

1. Agustí, A., MacNee, W., Donaldson, K., & Cosio, M. (2003). Hypothesis: does COPD have an autoimmune component? Thorax 58, 832-834.
2. Asokananthan, N., Graham, P. T., Stewart, D. J., Bakker, A. J., Eidne, K. A., Thompson, P. J., et al. (2002). House dust mite allergens induce proinflammatory cytokines from respiratory epithelial cells: the cysteine protease allergen, Der p 1, activates protease-activated receptor (PAR)-2 and inactivates PAR-1. J Immunol 169, 4572-4578.
3. Barends, M., de Rond, L. G., Dormans, J., van Oosten, M., Boelen, A., Neijens, H. J., et al. (2004). Respiratory syncytial virus, pneumonia virus of mice, and influenza A virus differently affect respiratory allergy in mice. Clin Exp Allergy 34, 488-496. (Pubitemid 38373014)
4. Barnes, P. J., & Celli, B. R. (2009). Systemic manifestations and comorbidities of COPD. Eur Respir J 33, 1165-1185.
5. Bartalesi, B., Cavarra, E., Fineschi, S., Lucattelli, M., Lunghi, B., Martorana, P. A., et al. (2005). Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur Respir J 25, 15-22. (Pubitemid 40207726)
6. Bartlett, N. W., Walton, R. P., Edwards, M. R., Aniscenko, J., Caramori, G., Zhu, J., et al. (2008). Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation. Nat Med 14, 199-204. (Pubitemid 351214556)
7. Bates, J. H., Cojocaru, A., Haverkamp, H. C., Rinaldi, L. M., & Irvin, C. G. (2008). The synergistic interactions of allergic lung inflammation and intratracheal cationic protein. Am J Respir Crit Care Med 177, 261-268. (Pubitemid 351198368)
8. Birrell, M. A., Battram, C. H., Woodman, P., McCluskie, K., & Belvisi, M. G. (2003). Dissociation by steroids of eosinophilic inflammation from airway hyperresponsiveness in murine airways. Respir Res 4, 3.
9. Birrell, M. A., McCluskie, K., Wong, S., Donnelly, L. E., Barnes, P. J., & Belvisi, M. G. (2005). Resveratrol, an extract of red wine, inhibits lipopolysaccharide induced airway neutrophilia and inflammatory mediators through an NF-kappaB-independent mechanism. FASEB J 19, 840-841. (Pubitemid 40617402)
10. Birrell, M. A., Wong, S., Hele, D. J., McCluskie, K., Hardaker, E., & Belvisi, M. G. (2005). Steroid-resistant inflammation in a rat model of chronic obstructive pulmonary disease is associated with a lack of nuclear factor-kappaB pathway activation. Am J Respir Crit Care Med 172, 74-84. (Pubitemid 40923317)
11. Borzone, G. R., Liberona, L. F., Bustamante, A. P., Saez, C. G., Olmos, P. R., Vecchiola, A., et al. (2009). Differences in lung glutathione metabolism may account for rodent susceptibility in elastase-induced emphysema development. Am J Physiol Regul Integr Comp Physiol 296, R1113-R1123.
12. Bramley, A. M., Khan, M. A., Manson, H. E., & Hegele, R. G. (2003). Development of respiratory syncytial virus "bronchiolitis" in guinea pigs does not reflect an allergic predisposition in the host. Chest 124, 671-681.
13. Brass, D. M., Hollingsworth, J. W., Cinque, M., Li, Z., Potts, E., Toloza, E., et al. (2008). Chronic LPS inhalation causes emphysema-like changes in mouse lung that are associated with apoptosis. Am J Respir Cell Mol Biol 39, 584-590.
14. Cates, E. C., Fattouh, R., Wattie, J., Inman, M. D., Goncharova, S., Coyle, A. J., et al. (2004). Intranasal exposure of mice to house dust mite elicits allergic airway inflammation via a GM-CSF-mediated mechanism. J Immunol 173, 6384-6392. (Pubitemid 39487798)
15. Cavarra, E., Bartalesi, B., Lucattelli, M., Fineschi, S., Lunghi, B., Gambelli, F., et al. (2001). Effects of cigarette smoke in mice with different levels of 1-proteinase inhibitor and sensitivity to oxidants. Am J Respir Crit Care Med 164, 886-890. (Pubitemid 32881929)
16. Chávez-Bueno, S., Mejías, A., Gómez, A. M., Olsen, K. D., Ríos, A. M., Fonseca-Aten, M., et al. (2005). Respiratory syncytial virus-induced acute and chronic airway disease is independent of genetic background: an experimental murine model. Virol J 2, 46.
17. Chin, C. L., Manzel, L. J., Lehman, E. E., Humlicek, A. L., Shi, L., Starner, T. D., et al. (2005). Haemophilus influenzae from patients with chronic obstructive pulmonary disease exacerbation induce more inflammation than colonizers. Am J Respir Crit Care Med 172, 85-91. (Pubitemid 40923318)
18. Church, D. F., & Pryor, W. A. (1985). Free-radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 64, 111-126. (Pubitemid 16135783)
19. Churg, A., & Wright, J. L. (2007). Animal models of cigarette smoke-induced chronic obstructive lung disease. Contrib Microbiol 14, 113-125.
20. Churg, A., Cosio, M., & Wright, J. L. (2008). Mechanisms of cigarette smoke-induced COPD: insights from animal models. Am J Physiol Lung Cell Mol Physiol 294, L612-L631. (Pubitemid 351520094)
21. Churg, A., Wang, R. D., Tai, H., Wang, X., Xie, C., & Wright, J. L. (2004). Tumor necrosis factor-alpha drives 70% of cigarette smoke-induced emphysema in the mouse. Am J Respir Crit Care Med 170, 492-498. (Pubitemid 39209129)
22. Curtis, J. L., Freeman, C. M., & Hogg, J. C. (2007). The immunopathogenesis of chronic obstructive pulmonary disease: insights from recent research. Proc Am Thorac Soc 4, 512-521.
23. Dakhama, A., Bramley, A. M., Chan, N. G., McKay, K. O., Schellenberg, R. R., & Hegele, R. G. (1999). Effect of respiratory syncytial virus on subsequent allergic sensitization to ovalbumin in guinea-pigs. Eur Respir J 13, 976-982. (Pubitemid 29288917)
24. De Alba, J., Raemdonck, K., Dekkak, A., Collins, M., Wong, S., Nials, A. T., et al. (2010). House dust mite induces direct airway inflammation in vivo: implications for future disease therapy? Eur Respir J 35, 1377-1387.
25. de Kluijver, J., Evertse, C. E., Sont, J. K., Schrumpf, J. A., & van Zeijl-van Test, C. J. (2003). Are rhinovirus-induced airway responses in asthma aggravated by chronic allergen exposure? Am J Respir Crit Care Med 168, 1174-1180.
26. Denzler, K. L., Borchers, M. T., Crosby, J. R., Cieslewicz, G., Hines, E. M., Justice, J. P., et al. (2001). Extensive eosinophil degranulation and peroxidase-mediated oxidation of airway proteins do not occur in a mouse ovalbumin-challenge model of pulmonary inflammation. J Immunol 167, 1672-1682. (Pubitemid 32703170)
27. D'hulst, A. I., Vermaelen, K. Y., Brusselle, G. G., Joos, G. F., & Pauwels, P. A. (2005). Time course of cigarette smoke-induced pulmonary inflammation in mice. Eur Respir J 26, 204-213.
28. Disis, M. L., Bernhard, H., Shiota, F. M., Han, S. L., Gralow, J. R., Huseby, E. S., et al. (1996). Granulocyte-macrophage colony-stimulating factor: an effective adjuvant for protein and peptide-based vaccines. Blood 88, 202-210. (Pubitemid 26230688)
29. Donaldson, G. C., Seemungal, T. A., Bhowmik, A., & Wedzicha, J. A. (2002). Relationship between exacerbation frequency and lung function decline in chronic obstructive pulmonary disease. Thorax 57, 847-852. (Pubitemid 35178607)
30. Dong, W., Selgrade, M. K., & Gilmour, M. I. (2003). Systemic administration of Bordetella pertussis enhances pulmonary sensitization to house dust mite in juvenile rats. Toxicol Sci 72, 113-121. (Pubitemid 36336440)
31. Dougherty, R. H., & Fahy, J. V. (2009). Acute exacerbations of asthma: epidemiology, biology and the exacerbation-prone phenotype. Clin Exp Allergy 39, 193-202.
32. Doz, E., Noulin, N., Boichot, E., Guénon, I., Fick, L., Le Bert, et al. (2008). Cigarette smoke-induced pulmonary inflammation is TLR4/MyD88 and IL-1R1/MyD88 signaling dependent. J Immunol 180, 1169-1178.
33. Drannik, A. G., Pouladi, M. A., Robbins, C. S., Goncharova, S. I., Kianpour, S., & Stampfli, M. R. (2004). Impact of cigarette smoke on clearance and inflammation after Pseudomonas aeruginosa infection. Am J Respir Crit Care Med 170, 1164-1171. (Pubitemid 39577373)
34. Eriksson, S. (1965). Studies in α1-antitrypsin deficiency. Acta Med Scand s432, 1-85.
35. Eum, S. Y., Maghni, K., Hamid, Q., Eidelman, D. H., Campbell, H., Isogai, S., et al. (2003). Inhibition of allergic airways inflammation and airway hyperresponsiveness in mice by dexamethasone: role of eosinophils, IL-5, eotaxin, and IL-13. J Allergy Clin Immunol 111, 1049-1061. (Pubitemid 36570866)
36. Evans, C. M., Fryer, A. D., Jacoby, D. B., Gleich, G. J., & Costello, R. W. (1997). Pretreatment with antibody to eosinophil major basic protein prevents hyperresponsiveness by protecting neuronal M2 muscarinic receptors in antigen-challenged guinea pigs. J Clin Invest 100, 2254-2262. (Pubitemid 27500148)
37. Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E., & Trifilieff, A. (2003). IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 170, 2106-2112. (Pubitemid 36197433)
38. Flood-Page, P., Menzies-Gow, A., Phipps, S., Ying, S., Wangoo, A., Ludwig, M. S., et al. (2003). Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics. J Clin Invest 112, 1029-1036. (Pubitemid 38056318)
39. Flood-Page, P., Swenson, C., Faiferman, I., Matthews, J., Williams, M., Brannick, L., et al. (2007). International Mepolizumab Study Group, A study to evaluate safety and efficacy of mepolizumab in patients with moderate persistent asthma. Am J Respir Crit Care Med 176, 1062-1071. (Pubitemid 350223751)
40. Foronjy, R. F., Mirochnitchenko, O., Propokenko, O., Lemaitre, V., Jia, Y., Inouye, M., et al. (2006). Superoxide Dismutase Expression Attenuates Cigarette Smoke- or Elastase-generated Emphysema in Mice. Am J Respir Crit Care Med 173, 623-631. (Pubitemid 43363803)
41. Fuchs, B., & Braun, A. (2008). Improved mouse models of allergy and allergic asthma - chances beyond ovalbumin. Curr Drug Targets 9, 495-502. (Pubitemid 352025206)
42. Fujisawa, T., Kato, Y., Nagase, H., Atsuta, J., Terada, A., Iguchi, K., et al. (2000). Chemokines induce eosinophil degranulation through CCR-3. J Allergy Clin Immunol 106, 507-513. (Pubitemid 32037703)
43. Fujita, M., Ye, Q., Ouchi, H., Nakashima, N., Hamada, N., Hagimoto, N., et al. (2004). Retinoic acid fails to reverse emphysema in adult mouse models. Thorax 59, 224-230. (Pubitemid 38339879)
44. Gaschler, G. J., Skrtic, M., Zavitz, C. C., Lindahl, M., Onnervik, P. O., Murphy, T. F., et al. (2009). Bacteria challenge in smoke-exposed mice exacerbates inflammation and skews the inflammatory profile. Am J Respir Crit Care Med 179, 666-675.
45. Gleich, G. J., Jacoby, D. B., & Fryer, A. D. (1995). Eosinophil-associated inflammation in bronchial asthma: a connection to the nervous system. Int Arch Allergy Immunol 107, 205-207.
46. Golovatch, P., Lemaitre, V., & D'Armiento, J. M. (2009). The development of emphysema in murine models of atherosclerosis. Am J Respir Crit Care Med 179, A1002.
47. Gosker, H. R., Langen, R. C., Bracke, K. R., Joos, G. F., Brusselle, G. G., Steele, C., et al. (2009). Extrapulmonary manifestations of chronic obstructive pulmonary disease in a mouse model of chronic cigarette smoke exposure. Am J Respir Cell Mol Biol 40, 710-716.
48. Graham, B. S., Perkins, M. D., Wright, P. F., & Karzon, D. T. (1988). Primary respiratory syncytial virus infection in mice. J Med Virol 26, 153-162.
49. Gregory, L. G., Causton, B., Murdoch, J. R., Mathie, S. A., O'Donnell, V., Thomas, C. P., et al. (2009). Inhaled house dust mite induces pulmonary T helper 2 cytokine production. Clin Exp Allergy 39, 1597-1610.
50. Gross, P., Pfitzer, E. A., Tolker, E., Babyak, M. A., & Kaschak, M. (1965). Experimental emphysema. Its production with papain in normal and silicotic rats. Arch Environ Health 11, 50-58.
51. Gualano, R. C., Hansen, M. J., Vlahos, R., Jones, J. E., Park-Jones, R. A., Deliyannis, G., et al. (2008). Cigarette smoke worsens lung inflammation and impairs resolution of influenza infection in mice. Respir Res 9, 53.
52. Guerassimov, A., Hoshino, Y., Takubo, Y., Turcotte, A., Yamamoto, M., Ghezzo, H., et al. (2004). The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am J Respir Crit Care Med 170, 974-980. (Pubitemid 39425693)
53. Haldar, P., Brightling, C. E., Hargadon, B., Gupta, S., Monteiro, W., Sousa, A., et al. (2009). Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med 360, 973-984.
54. Hall, C. B. (2001). Respiratory syncytial virus and parainfluenza virus. N Engl J Med 344, 1917-1928.
55. Hammad, H., Chieppa, M., Perros, F., Willart, M. A., Germain, R. N., & Lambrecht, B. N. (2009). House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 15, 410-416.
56. Hashimoto, K., Graham, B. S., Ho, S. B., Adler, K. B., Collins, R. D., Olson, S. J., et al. (2004). Respiratory syncytial virus in allergic lung inflammation increases Muc5ac and gob-5. Am J Respir Crit Care Med 170, 306-312. (Pubitemid 38971416)
57. Hautamaki, R. D., Kobayashi, D. K., Senior, R. M., & Shapiro, S. D. (1997). Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 277, 2002-2004. (Pubitemid 27449144)
58. Hegele, R. G., Robinson, P. J., Gonzalez, S., & Hogg, J. C. (1993). Production of acute bronchiolitis in guinea-pigs by human respiratory syncytial virus. Eur Respir J 6, 1324-1331. (Pubitemid 23329549)
59. Henrickson, K. J., Hoover, S., Kehl, K. S., & Hua, W. (2004). National disease burden of respiratory viruses detected in children by polymerase chain reaction. Pediatr Infect Dis J 23, S11-S18. (Pubitemid 38168906)
60. Hogg, J. C., Chu, F., Utokaparch, S., Woods, R., Elliott, W. M., Buzatu, L., et al. (2004). The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 350, 2645-2653. (Pubitemid 38787999)
61. Houghton, A. M., Quintero, P. A., Perkins, D. L., Kobayashi, D. K., Kelley, D. G., Marconcini, L. A., et al. (2006). Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest 116, 753-759. (Pubitemid 43326884)
62. Ishii, A., Takaoka, M., & Matsui, Y. (1977). Production of guinea pig reaginic antibody against the house dust mite extract, Dermatophagoides pteronyssinus, without adjuvant. Jpn J Exp Med 47, 377-383. (Pubitemid 8237023)
63. Ishii, Y., Itoh, K., Morishima, Y., Kimura, T., Kiwamoto, T., Iizuka, T., et al. (2005). Transcription factor Nrf2 plays a pivotal role in protection against elastase-induced pulmonary inflammation and emphysema. J Immunol 15, 6968-6975. (Pubitemid 41598943)
64. Ito, K., Herbert, C., Siegle, J. S., Vuppusetty, C., Hansbro, N., Thomas, P. S., et al. (2008). Steroid-resistant neutrophilic inflammation in a mouse model of an acute exacerbation of asthma. Am J Respir Cell Mol Biol 39, 543-550.
65. Ito, K., Ito, M., Elliott, W. M., Cosio, B., Caramori, G., Kon, O. M., et al. (2005). Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 352, 1967-1976. (Pubitemid 40638367)
66. Jackson, D. J., Gangnon, R. E., Evans, M. D., Roberg, K. A., Anderson, E. L., Pappas, T. E., et al. (2008). Wheezing rhinovirus illnesses in early life predict asthma development in high-risk children. Am J Respir Crit Care Med 178, 667-672.
67. Jobse, B. N., Johnson, J. R., Farncombe, T. H., Labiris, R., Walker, T. D., Goncharova, S., et al. (2009). Evaluation of allergic lung inflammation by computed tomography in a rat model in vivo. Eur Respir J 33, 1437-1447.
68. Johnson, J. R., Wiley, R. E., Fattouh, R., Swirski, F. K., Gajewska, B. U., Coyle, A. J., et al. (2004). Continuous exposure to house dust mite elicits chronic airway inflammation and structural remodelling. Am J Respir Crit Care Med 169, 378-385.
69. Johnson, J. R., Pacitto, S. R., Wong, J., Archer, E. W., Eirefelt, S., Miller-Larsson, A., et al. (2008). Combined budesonide/formoterol therapy in conjunction with allergen avoidance ameliorates house dust mite-induced airway remodeling and dysfunction. Am J Physiol Lung Cell Mol Physiol 295, L780-L788.
70. Johnston, S. L., Pattemore, P. K., Sanderson, G., Smith, S., Lampe, F., Josephs, L., et al. (1995). Community study of role of viral infections in exacerbations of asthma in 9-11 year old children. BMJ 310, 1225-1229.
71. Kang, M. J., Lee, C. G., Lee, J. Y., Dela Cruz, C. S., Chen, Z. J., Enelow, R., et al. (2008). Cigarette smoke selectively enhances viral PAMP- and virus-induced pulmonary innate immune and remodeling responses in mice. J Clin Invest 118, 2771-2784.
72. Kaplan, P. D., Kuhn, C., & Pierce, J. A. (1973). The induction of emphysema with elastase. I. The evolution of the lesion and the influence of serum. J Lab Clin Med 82, 349-356.
73. King, C., Brennan, S., Thompson, P. J., & Stewart, G. A. (1998). Dust mite proteolytic allergens induce cytokine release from cultured airway epithelium. J Immunol 161, 3645-3651.
74. Kondo, Y., Matsuse, H., Machida, I., Kawano, T., Saeki, S., Tomari, S., et al. (2004). Effects of primary and secondary low-grade respiratory syncytial virus infections in a murine model of asthma. Clin Exp Allergy 34, 1307-1313. (Pubitemid 39093073)
75. Kuhn, C., Yu, S. Y., Chraplyvy, M., Linder, H. E., & Senior, R. M. (1976). The induction of emphysema with elastase. II. Changes in connective tissue. Lab Invest 34, 372-380.
76. Kumar, R. K., Herbert, C., & Kasper, M. (2004). Reversibility of airway inflammation and remodelling following cessation of antigenic challenge in a model of chronic asthma. Clin Exp Allergy 34, 1796-1802. (Pubitemid 39551536)
77. Kuraki, T., Ishibashi, M., Takayama, M., Shiraishi, M., & Yoshida, M. (2002). A novel oral neutrophil elastase inhibitor (ONO-6818) inhibits human neutrophil elastase-induced emphysema in rats. Am J Respir Crit Care Med 166, 496-500.
78. Laurell, C. -B., & Eriksson, S. (1963). The electrophoretic α1-globulin pattern of serum in α1-antitrypsin deficiency. Scand J Clin Lab Invest 15, 132-140.
79. Lee, J. J., Dimina, D., Macias, M. P., Ochkur, S. I., McGarry, M. P., O'Neill, K. R., et al. (2004). Defining a link with asthma in mice congenitally deficient in eosinophils. Science 305, 1773-1776. (Pubitemid 39249644)
80. Lee, K. K., Hegele, R. G., Manfreda, J., Wooldrage, K., Becker, A. B., Ferguson, A. C., et al. (2007). Relationship of early childhood viral exposures to respiratory symptoms, onset of possible asthma and atopy in high risk children: the Canadian Asthma Primary Prevention Study. Pediatr Pulmonol 42, 290-297. (Pubitemid 46417704)
81. Legg, J. P., Hussain, I. R., Warner, J. A., Johnston, S. L., & Warner, J. O. (2003). Type 1 and type 2 cytokine imbalance in acute respiratory syncytial virus bronchiolitis. Am J Respir Crit Care Med 168, 633-639. (Pubitemid 37175965)
82. Lemanske, R. F., Jr., Jackson, D. J., Gangnon, R. E., Evans, M. D., Li, Z., Shult, P. A., et al. (2005). Rhinovirus illnesses during infancy predict subsequent childhood wheezing. J Allergy Clin Immunol 116, 571-577. (Pubitemid 41267130)
83. Leme, A. S., Berndt, B., Williams, L. K., Paigen, B., & Shapiro, S. D. (2009). Interstrain variability on the development of emphysema in cigarette smoke-exposed mice. Am J Respir Crit Care Med 179, A1008.
84. Lucey, E. C., Keane, J., Kuang, P. P., Snider, G. L., & Goldstein, R. H. (2002). Severity of elastase-induced emphysema is decreased in tumor necrosis factor-alpha and interleukin-1beta receptor-deficient mice. Lab Invest 82, 79-85. (Pubitemid 34072648)
85. Lucey, E. C., Goldstein, R. H., Breuer, R., Rexer, B. N., Ong, D. E., & Snider, G. L. (2003). Retinoic acid does not affect alveolar septation in adult FVB mice with elastase-induced emphysema. Respiration 70, 200-205. (Pubitemid 36578790)
86. Lukacs, N. W., Tekkanat, K. K., Berlin, A., Hogaboam, C. M., Miller, A., Evanoff, H., et al. (2001). Respiratory syncytial virus predisposes mice to augmented allergic airway responses via IL-13-mediated mechanisms. J Immunol 167, 1060-1065. (Pubitemid 32660865)
87. Lukacs, N. W., Moore, M. L., Rudd, B. D., Berlin, A. A., Collins, R. D., Olson, S. J., et al. (2006). Differential immune responses and pulmonary pathophysiology are induced by two different strains of respiratory syncytial virus. Am J Pathol 169, 977-986. (Pubitemid 44411960)
88. Maes, T., Bracke, K. R., Vermaelen, K. Y., Demedts, I. K., Joos, G. F., Pauwels, R. A., et al. (2006). Murine TLR4 is implicated in cigarette smoke-induced pulmonary inflammation. Int Arch Allergy Immunol 141, 354-368. (Pubitemid 44783906)
89. Mahadeva, R., & Shapiro, S. D. (2002). Chronic obstructive pulmonary disease * 3: Experimental animal models of pulmonary emphysema. Thorax 57, 908-914. (Pubitemid 35178618)
90. Makris, D., Moschandreas, J., Damianaki, A., Ntaoukakis, E., Siafakas, N. M., Milic Emili, J., et al. (2007). Exacerbations and lung function decline in COPD: new insights in current and ex-smokers. Respir Med 101, 1305-1312. (Pubitemid 46667662)
91. Maksvytis, H. J., Vaccaro, C., & Brody, J. S. (1981). Isolation and characterization of the lipid-containing interstitial cell from the developing rat lung. Lab Invest 45, 248-259. (Pubitemid 11000170)
92. March, T. H., Cossey, P. Y., Esparza, D. C., Dix, K. J., McDonald, J. D., & Bowen, L. E. (2004). Inhalation administration of all-trans-retinoic acid for treatment of elastase-induced pulmonary emphysema in Fischer 344 rats. Exp Lung Res 30, 383-404.
93. Marwick, J. A., Kirkham, P. A., Stevenson, C. S., Danahay, H., Giddings, J., Butler, K., et al. (2004). Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 31, 633-642. (Pubitemid 39587493)
94. Marwick, J. A., Caramori, G., Stevenson, C. S., Casolari, P., Jazrawi, E., Barnes, P. J., et al. (2009). Inhibition of PI3K{delta} restores glucocorticoid function in smoking-induced airway inflammation in mice. Am J Respir Crit Care Med 179, 542-548.
95. Massaro, G. D., & Massaro, D. (1997). Retinoic acid treatment abrogates elastase-induced pulmonary emphysema in rats. Nat Med 3, 675-677.
96. Maunsell, K., Wraith, D. G., & Cunnington, A. M. (1968). Mites and house-dust allergy in bronchial asthma. Lancet, 1267-1270.
97. McAllen, M. K., Assem, E. S., & Maunsell, K. (1970). House-dust mite asthma, results of challenge tests on five criteria with Dermatophagoides pteronyssinus. Br Med J 2, 501-504.
98. McAllister, D. A., Maclay, J. D., Mills, N. L., Mair, G., Miller, J., Anderson, D., et al. (2007). Arterial stiffness is independently associated with emphysema severity in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176, 1208-1214. (Pubitemid 350256474)
99. McGowan, S. E., Harvey, C. S., & Jackson, S. K. (1995). Retinoids, retinoic acid receptors, and cytoplasmic retinoid binding proteins in perinatal rat lung fibroblasts. Am J Physiol 269, L463-L472.
100. McGowan, S., Jackson, S. K., Jenkins-Moore, M., Dai, H. H., Chambon, P., & Snyder, J. M. (2000). Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am J Respir Cell Mol Biol 23, 162-167. (Pubitemid 30656424)
101. McMillan, S. J., & Lloyd, C. M. (2004). Prolonged allergen challenge in mice leads to persistent airway remodelling. Clin Exp Allergy 34, 497-507. (Pubitemid 38373015)
102. Menzies-Gow, A., Ying, S., Sabroe, I., Stubbs, V. L., Soler, D., Williams, T. J., et al. (2002). Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early- and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J Immunol 169, 2712-2718.
103. Mertens, V. E. (1930). Preliminary report on cigarette smoke as possible cause of cancer of lungs. Ztschi f Kreboforsch 32, 1291.
104. Meshi, B., Vitalis, T. Z., Ionescu, D., Elliott, W. M., Liu, C., Wang, X. D., et al. (2002). Emphysematous lung destruction by cigarette smoke. The effects of latent adenoviral infection on the lung inflammatory response. Am J Respir Cell Mol Biol 26, 52-57. (Pubitemid 34029820)
105. Modestou, M. A., Manzel, L. J., El-Mahdy, S., & Look, D. C. (2010). Inhibition of IFN-gamma-dependent antiviral airway epithelial defense by cigarette smoke. Respir Res 11, 64.
106. Monick, M. M., Yarovinsky, T. O., Powers, L. S., Butler, N. S., Carter, A. B., Gudmundsson, G., et al. (2003). Respiratory syncytial virus up-regulates TLR4 and sensitizes airway epithelial cells to endotoxin. J Biol Chem 278, 53035-53044. (Pubitemid 38035906)
107. Morris, A., Kinnear, G., Wan, W. Y., Wyss, D., Bahra, P., & Stevenson, C. S. (2008). Comparison of cigarette smoke-induced acute inflammation in multiple strains of mice and the effect of a matrix metalloproteinase inhibitor on these responses. J Pharmacol Exp Ther 327, 851-862.
108. Morrissey, P. J., Bressler, L., Park, L. S., Alpert, A., & Gillis, S. (1987). Granulocyte-macrophage colony-stimulating factor augments the primary antibody response by enhancing the function of antigen-presenting cells. J Immunol 139, 1113-1119. (Pubitemid 17125060)
109. Nadziejko, C., Fang, K., Bravo, A., & Gordon, T. (2007). Susceptibility to pulmonary hypertension in inbred strains of mice exposed to cigarette smoke. J Appl Physiol 102, 1780-1785. (Pubitemid 46701944)
110. National Heart, Lung, and Blood Institute (1997). National Asthma Education and Prevention Program Expert Panel Report 2. Guidelines for the Diagnosis and Management of Asthma. Bethesda.
111. Newcomb, D. C., & Peebles, R. S., Jr. (2009). Bugs and asthma: a different disease? Proc Am Thorac Soc 6, 266-271.
112. Noble, V., Murray, M., Webb, M. S. C., Alexander, J., Swarbrick, A. S., & Milner, A. D. (1997). Respiratory status and allergy nine to 10 years after acute bronchiolitis. Arch Dis Child 76, 315-319. (Pubitemid 27174540)
113. Ochkur, S. I., Jacobsen, E. A., Protheroe, C. A., Biechele, T. L., Pero, R. S., McGarry, M. P., et al. (2007). Coexpression of IL-5 and eotaxin-2 in mice creates an eosinophil-dependent model of respiratory inflammation with characteristics of severe asthma. J Immunol 178, 7879-7889. (Pubitemid 46898060)
114. Ofulue, A. F., Ko, M., & Abboud, R. T. (1998). Time course of neutrophil and macrophage elastinolytic activities in cigarette smoke-induced emphysema. Am J Physiol 275, L1134-L1144.
115. Peebles, R. S., Jr., Sheller, J. R., Johnson, J. E., Mitchell, D. B., & Graham, B. S. (1999). Respiratory syncytial virus infection prolongs methacholine-induced airway hyperresponsiveness in ovalbumin-sensitized mice. J Med Virol 57, 186-192. (Pubitemid 29022513)
116. Peebles, R. S., Jr., Hashimoto, K., Collins, R. D., Jarzecka, K., Furlong, J., Mitchell, D. B., et al. (2001). Immune interaction between respiratory syncytial virus infection and allergen sensitization critically depends on timing of challenges. J Infect Dis 184, 1374-1379. (Pubitemid 33108850)
117. Pemberton, P. A., Cantwell, J. S., Kim, K. M., Sundin, D. J., Kobayashi, D., Fink, J. B., et al. (2005). An inhaled matrix metalloprotease inhibitor prevents cigarette smoke-induced emphysema in the mouse. COPD 2, 303-310. (Pubitemid 43879446)
118. Phipps, S., Lam, C. E., Kaiko, G. E., Foo, S. Y., Collison, A., Mattes, J., et al. (2009). Toll/IL-1 signaling is critical for house dust mite-specific helper T cell type 2 and type 17 [corrected] responses. Am J Respir Crit Care Med 179, 883-893.
119. Platt-Mills, T. A. (1995). The role of indoor allergens in asthma. Allergy 50, 5.
120. Prince, G. A., Jenson, A. B., Horswood, R. L., Camargo, E., & Chanock, R. M. (1978). The pathogenesis of respiratory syncytial virus infection in cotton rats. Am J Pathol 93, 771-791. (Pubitemid 9087309)
121. Rabe, K. F., Hurd, S., Anzueto, A., Barnes, P. J., Buist, S. A., Calverley, P., et al. (2007). Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 176, 532-555. (Pubitemid 47403272)
122. Rangasamy, T., Cho, C. Y., Thimmulappa, R. K., Zhen, L., Srisuma, S. S., Kensler, T. W., et al. (2004). Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 114, 1248-1259. (Pubitemid 40385296)
123. Rennard, S. I., Fogarty, C., Kelsen, S., Long, W., Ramsdell, J., Allison, J., et al. (2007). The safety and efficacy of infliximab in moderate to severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 175, 926-934. (Pubitemid 46684703)
124. Robbins, C. S., Bauer, C. M., Vujicic, N., Gaschler, G. J., Lichty, B. D., Brown, E. G., et al. (2006). Cigarette smoke impacts immune inflammatory responses to influenza in mice. Am J Respir Crit Care Med 174, 1342-1351. (Pubitemid 44913036)
125. Robinson, P. J., Hegele, R. G., & Schellenberg, R. R. (1997). Allergic sensitization increases airway reactivity in guinea pigs with respiratory syncytial virus bronchiolitis. J Allergy Clin Immunol 100, 492-498. (Pubitemid 27441306)
126. Roth, M. D., Connett, J. E., D'Armiento, J. M., Foronjy, R. F., Friedman, P. J., Goldin, J. G., et al. (2006). Feasibility of retinoids for the treatment of emphysema study. Chest 130, 1334-1345. (Pubitemid 44786724)
127. Rubio, M. L., Martin-Mosquero, M. C., Ortega, M., Peces-Barba, G., & Gonzalez-Mangado, N. (2004). Oral N-acetylcysteine attenuates elastase-induced pulmonary emphysema in rats. Chest 125, 1500-1506. (Pubitemid 38501368)
128. Salvi, S. S., & Barnes, P. J. (2009). Chronic obstructive pulmonary disease in non-smokers. Lancet 374, 733-743.
129. Savov, J. D., Brass, D. M., Berman, K. G., McElvania, E., & Schwartz, D. A. (2003). Fibrinolysis in LPS-induced chronic airway disease. Am J Physiol Lung Cell Mol Physiol 285, L940-L948. (Pubitemid 37158842)
130. Schauer, U., Hoffjan, S., Bittscheidt, J., Köchling, A., Hemmis, S., Bongartz, S., et al. (2002). RSV bronchiolitis and risk of wheeze and allergic sensitisation in the first year of life. Eur Respir J 20, 1277-1283. (Pubitemid 35331889)
131. Schols, A. M., Broekhuizen, R., Weling-Scheepers, C. A., & Wouters, E. F. (2005). Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr 82, 53-59. (Pubitemid 41716377)
132. Schwarze, J., Hamelmann, E., Bradley, K. L., Takeda, K., & Gelfand, E. W. (1997). Respiratory syncytial virus infection results in airway hyperresponsiveness and enhanced airway sensitization to allergen. J Clin Invest 100, 226-233. (Pubitemid 27311261)
133. Shapiro, S. D., Demeo, D. L., & Silverman, E. K. (2004). Smoke and mirrors: mouse models as a reflection of human chronic obstructive pulmonary disease. Am J Respir Crit Care Med 170, 929-931. (Pubitemid 39425685)
134. Sigurs, N. (2002). A cohort of children hospitalised with acute RSV bronchiolitis: impact on later respiratory disease. Paediatr Respir Rev 3, 177-183.
135. Sigurs, N., Bjarnason, R., Sigurbergsson, F., Kjellman, B., & Björkstén, B. (1995). Asthma and immunoglobulin E antibodies after respiratory syncytial virus bronchiolitis: a prospective cohort study with matched controls. Pediatrics 95, 500-505.
136. Sigurs, N., Gustafsson, P. M., Bjarnason, R., Lundberg, F., Schmidt, S., Sigurbergsson, F., et al. (2005). Severe respiratory syncytial virus bronchiolitis in infancy and asthma and allergy at age 13. Am J Respir Crit Care Med 171, 137-141. (Pubitemid 40105412)
137. Sin, D. D., Anthonisen, N. R., Soriano, J. B., & Agusti, A. G. (2006). Mortality in COPD: Role of comorbidities. Eur Respir J 28, 1245-1257. (Pubitemid 44883863)
138. Singh, A. M., & Busse, W. W. (2006). Asthma exacerbations. 2: aetiology. Thorax 61, 809-816.
139. Singh, P., Daniels, M., Winsett, D. W., Richards, J., Doerfler, D., Hatch, G., et al. (2003). Phenotypic comparison of allergic airway responses to house dust mite in three rat strains. Am J Physiol Lung Cell Mol Physiol 284, L588-L598. (Pubitemid 36343307)
140. Stämpfli, M. R., Wiley, R. E., Neigh, G. S., Gajewska, B. U., Lei, X. F., Snider, D. P., et al. (1998). GM-CSF transgene expression in the airway allows aerosolized ovalbumin to induce allergic sensitization in mice. J Clin Invest 102, 1704-1714.
141. Stein, R. T., Sherrill, D., Morgan, W. J., Holberg, C. J., Halonen, M., Taussig, L. M., et al. (1999). Respiratory syncytial virus in early life and risk of wheeze and allergy by age 13 years. Lancet 354, 541-545. (Pubitemid 29381367)
142. Stevenson, C. S., & Belvisi, M. G. (2008). Preclinical animal models of asthma and chronic obstructive pulmonary disease. Expert Rev Respir Med 2, 631-643.
143. Stevenson, C. S., Docx, C., Webster, R., Battram, C., Hynx, D., Giddings, J., et al. (2007). Comprehensive gene expression profiling of rat lung reveals distinct acute and chronic responses to cigarette smoke inhalation. Am J Physiol Lung Cell Mol Physiol 293, L1183-L1193. (Pubitemid 350159403)
144. Stolk, J., Rudolphus, A., Davies, P., Osinga, D., Dijkman, J. H., Agarwal, L., et al. (1992). Induction of emphysema and bronchial mucus cell hyperplasia by intratracheal instillation of lipopolysaccharide in the hamster. J Pathol 167, 349-356.
145. -/--mice by different pathways. Toxicol Lett 180, S40-S41.
146. Sun, G., Stacey, M. A., Schmidt, M., Mori, L., & Mattoli, S. (2001). Interaction of mite allergens Der p3 and Der p9 with protease-activated receptor-2 expressed by lung epithelial cells. J Immunol 167, 1014-1021. (Pubitemid 32660859)
147. Sussan, T. E., Rangasamy, T., Blake, D. J., Malhotra, D., El-Haddad, H., Bedja, D., et al. (2009). Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc Natl Acad Sci USA 106, 250-255.
148. Swirski, F. K., Sajic, D., Robbins, C. S., Gajewska, B. U., Jordana, M., & Stämpfli, M. R. (2002). Chronic exposure to innocuous antigen in sensitized mice leads to suppressed airway eosinophilia that is reversed by granulocyte macrophage colony-stimulating factor. J Immunol 169, 3499-3506.
149. Takahashi, S., Nakamura, H., Seki, M., Shiraishi, Y., Yamamoto, M., Furuuchi, M., et al. (2008). Reversal of elastase-induced pulmonary emphysema and promotion of alveolar epithelial cell proliferation by simvastatin in mice. Am J Physiol Lung Cell Mol Physiol 294, L882-L890.
150. Tanaka, H., Komai, M., Nagao, K., Ishizaki, M., Kajiwara, D., Takatsu, K., et al. (2004). Role of interleukin-5 and eosinophils in allergen-induced airway remodeling in mice. Am J Respir Cell Mol Biol 31, 62-68. (Pubitemid 38888040)
151. Tang, K., Wagner, P. D., & Breen, E. C. (2010). TNF-alpha-mediated reduction in PGC-1alpha may impair skeletal muscle function after cigarette smoke exposure. J Cell Physiol 222, 320-327.
152. Temelkovski, J., Hogan, S. P., Shepherd, D. P., Foster, P. S., & Kumar, R. K. (1998). An improved murine model of asthma: selective airway inflammation, epithelial lesions and increased methacholine responsiveness following chronic exposure to aerosolised allergen. Thorax 53, 849-856. (Pubitemid 28459541)
153. Therien, A. G., Bernier, V., Weicker, S., Tawa, P., Falgueyret, J. P., Mathieu, M. C., et al. (2008). Adenovirus IL-13-induced airway disease in mice: a corticosteroid-resistant model of severe asthma. Am J Respir Cell Mol Biol 39, 26-35. (Pubitemid 351883955)
154. Thomas, W. R., Smith, W. A., Hales, B. J., Mills, K. L., & O'Brien, R. M. (2002). Characterization and immunobiology of house dust mite allergens. Int Arch Allergy Immunol 129, 1-18. (Pubitemid 35316844)
155. Tourdot, S., Mathie, S., Hussell, T., Edwards, L., Wang, H., Openshaw, P. J., et al. (2008). Respiratory syncytial virus infection provokes airway remodelling in allergen-exposed mice in absence of prior allergen sensitization. Clin Exp Allergy 38, 1016-1024. (Pubitemid 351725848)
156. Trompette, A., Divanovic, S., Visintin, A., Blanchard, C., Hegde, R. S., Madan, R., et al. (2009). Allergenicity resulting from functional mimicry of a Toll-like receptor complex protein. Nature 457, 585-588.
157. Ulrich, K., Hincks, J. S., Walsh, R., Wetterstrand, E. M., Fidock, M. D., Sreckovic, S., et al. (2008). Anti-inflammatory modulation of chronic airway inflammation in the murine house dust mite model. Pulm Pharmacol Ther 21, 637-647. (Pubitemid 351970713)
158. van der Strate, B. W., Postma, D. S., Brandsma, C. A., Melgert, B. N., Luinge, M. A., Geerlings, M., et al. (2006). Cigarette smoke-induced emphysema: a role for the B cell? Am J Respir Crit Care Med 173, 751-758.
159. van der Vaart, H., Koeter, G. H., Postma, D. S., Kauffman, H. F., & ten Hacken, N. H. (2005). First study of infliximab treatment in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 172, 465-469.
160. Van Hove, C. L., Maes, T., Joos, G. F., & Tournoy, K. G. (2007). Prolonged inhaled allergen exposure can induce persistent tolerance. Am J Respir Cell Mol Biol 36, 573-584. (Pubitemid 46676716)
161. Van Hove, C. L., Maes, T., Cataldo, D. D., Guéders, M. M., Palmans, E., Joos, G. F., et al. (2009). Comparison of acute inflammatory and chronic structural asthma-like responses between C57BL/6 and BALB/c mice. Int Arch Allergy Immunol 149, 195-207.
162. Vlahos, R., Bozinovski, S., Jones, J. E., Powell, J., Gras, J., Lilja, A., et al. (2006). Differential protease, innate immunity, and NF-kappaB induction profiles during lung inflammation induced by subchronic cigarette smoke exposure in mice. Am J Physiol Lung Cell Mol Physiol 290, L931-L945. (Pubitemid 43725055)
163. Wakahara, K., Tanaka, H., Takahashi, G., Tamari, M., Nasu, R., Toyohara, T., et al. (2008). Repeated instillations of Dermatophagoides farinae into the airways can induce Th2-dependent airway hyperresponsiveness, eosinophilia and remodeling in mice: effect of intratracheal treatment of fluticasone propionate. Eur J Pharmacol 578, 87-96. (Pubitemid 350179752)
164. Wan, W. Y., Morris, A., Kinnear, G., Pearce, W., Mok, J., Wyss, D., et al. (2010). Pharmacological characterisation of anti-inflammatory compounds in acute and chronic mouse models of cigarette smoke-induced inflammation. Respir Res 11, 126.
165. Wenzel, S., & Holgate, S. T. (2006). The mouse trap: it still yields few answers in asthma. Am J Respir Crit Care Med 174, 1173-1176 discussion 1176-1178.
166. World Health Organisation (2008a). Fact Sheet No. 307. http://www.who.int/mediacentre/factsheets/fs307/en/index.html.
167. World Health, Organisation (2008b). Fact Sheet No. 315. http://www.who.int/mediacentre/factsheets/fs315/en/index.html.
168. Wright, J. L., & Churg, A. (1990). Cigarette smoke causes physiologic and morphologic changes of emphysema in the guinea pig. Am Rev Respir Dis 142, 1422-1428.
169. Wright, J. L., & Churg, A. (1991). Effect of long-termcigarette smoke exposure on pulmonary vascular structure and function in the guinea pig. Exp Lung Res 17, 997-1009.
170. Wright, J. L., Postma, D. S., Kerstjens, H. A., Timens, W., Whittaker, P., & Churg, A. (2007). Airway remodeling in the smoke exposed guinea pig model. Inhal Toxicol 19, 915-923. (Pubitemid 350112226)
171. Wyss, D., Bonneau, O., & Trifilieff, A. (2007). Synergistic effect of formoterol and mometasone in a mouse model of allergic lung inflammation. Br J Pharmacol 152, 83-90. (Pubitemid 47339912)
172. Yasue, M., Yokota, T., Okudaira, H., & Okumura, Y. (1999). Induction of allergic reactions in guinea pigs with purified house dust mite allergens. Cell Immunol 192, 185-193. (Pubitemid 29172085)
173. Yin, F. H., & Lomax, N. B. (1986). Establishment of a mouse model for human rhinovirus infection. J Gen Virol 67, 2335-2340. (Pubitemid 17179527)
174. You, D., Becnel, D., Wang, K., Ripple, M., Daly, M., & Cormier, S. A. (2006). Exposure of neonates to respiratory syncytial virus is critical in determining subsequent airway response in adults. Respir Res 7, 107.
175. Zhu, Z., Homer, R. J., Wang, Z., Chen, Q., Geba, G. P., Wang, J., et al. (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 103, 779-788. (Pubitemid 29152623)
176. Zosky, G. R., & Sly, P. D. (2007). Animal models of asthma. Clin Exp Allergy 37, 973-988. (Pubitemid 46955517)