Advanced search
Publication Cover
Expert Review of Respiratory Medicine Volume 4, 2010 - Issue 6
Submit an article Journal homepage
385
Views
49
CrossRef citations to date
0
Altmetric
Special Report

Animal models of cigarette smoke-induced chronic obstructive pulmonary disease

Joanne L Wright Department of Pathology, University Hospital, University of British Columbia, 2211 Wesbrook Mall, Vancouver, BC V6T 2B5, Canada;[email protected]
&
Andrew Churg Department of Pathology, University Hospital, University of British Columbia, 2211 Wesbrook Mall, Vancouver, BC V6T 2B5, Canada; Department of Pathology, University Hospital, University of British Columbia, 2211 Wesbrook Mall, Vancouver, BC V6T 2B5, Canada
Pages 723-734 | Published online: 09 Jan 2014

References

  • Churg A, Cosio M, Wright JL. Mechanisms of cigarette smoke-induced COPD: insights from animal models. Am. J. Physiol.294, L612–L631 (2008).
  • McGowan SE, Snyder JM. Development of alveoli. In: The Lung: Development, Aging and the Environment. Harding R, Pinkerton KE, Plopper CG (Eds). Elsevier Academic Press, London, UK, 55–73 (2004).
  • Hsia CCW, Johnson RL, Weibel ER. Compensatory lung growth: relationship to postnatal lung growth and adaption in destructive lung disease. In: The Lung: Development, Aging and the Environment. Harding R, Pinkerton KE, Plopper CG (Eds). Elsevier Academic Press, London, UK, 187–199 (2004).
  • Plopper CG, Mango GW, Hatch GE et al. Elevation of susceptibility to ozone-induced acute tracheobronchial injury in transgenic mice deficient in Clara cell secretory protein. Toxicol. Appl. Pharm.213, 74–85 (2006).
  • Rahman I, Biswas SK, Kode A. Oxidant and antioxidant balance in the airways and airway diseases. Eur. J. Pharmacol.533, 222–239 (2006).
  • Guerassimov A, Hoshino M, Takubo Y et al. The development of emphysema in cigarette smoke-exposed mice is strain dependent. Am. J. Respir. Crit. Care Med.170, 974–980 (2005).
  • Roh GS, Yi CO, Cho YJ et al. Anti-inflammatory effects of celecoxib in rat lungs with smoke-induced emphysema. Am. J. Physiol.(2010) (In press).
  • MacNee W, Rahman I. Is oxidative stress central to the pathogenesis of chronic obstructive pulmonary disease? Trends Mol. Med.7, 55–62 (2001).
  • Rahman I, MacNee W. Role of oxidants/antioxidants in smoking-induced lung diseases. Free Radic. Biol. Med.21, 669–681 (1996).
  • Foronjy RF, Mirochnitchenko O, Propokenko A et al. Superoxide dismutase expression attenuates cigarette smoke- or elastase-generated emphysema in mice. Am. J. Respir. Crit. Care Med.173, 623–631 (2006).
  • Sussan TE, Rangasamy T, Blake DJ et al. Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice. Proc. Natl Acad. Sci. USA106, 250–255 (2009).
  • Yoshida T, Mett I, Bhunia AK et al. Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat. Med.16, 767–774 (2010).
  • Rajendrasozhan S, Chung S, Sundar IK, Yao H, Rahman I. Targeted disruption of NF-κB1 (p50) augments cigarette smoke-induced lung inflammation and emphysema in mice: a critical role of p50 in chromatin remodeling. Am. J. Physiol.298, 197–209 (2010).
  • Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N. Engl. J. Med.360, 2445–2454 (2009).
  • Pemberton PA, Cantwell JS, Kim KM et al. An inhaled matrix metalloprotease inhibitor prevents cigarette smoke-induced emphysema in the mouse. COPD3, 303–310 (2005).
  • Churg A, Wang RD, Tai H, Wang X, Xie C, Wright JL. Tumor necrosis factor-α drives 70% of cigarette smoke-induced emphysema in the mouse. Am. J. Respir. Crit. Care Med.170, 492–498 (2004).
  • D’hulst AI, Bracke KR, Maes T et al. Role of tumour necrosis factor-α receptor p75 in cigarette smoke-induced pulmonary inflammation and emphysema. Eur. Respir. J.28, 102–112 (2006).
  • Barnes PJ. Unexpected failure of anit-tumor necrosis factor therapy in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.175, 866–867 (2007).
  • Martorana PA, Beume R, Lucattelli M, Wollin L, Lungarella G. Roflumilast fully prevents emphysema in mice chronically exposed to cigarette smoke. Am. J. Respir. Crit. Care Med.172, 848–853 (2005).
  • Fabbri LM, Calverley P, Izquierdo-Alonso JL et al. Roflumilast in moderate-to-severe chronic obstructive pulmonary disease treated with longacting bronchodilators: two randomised clinical trials. Lancet374, 695–703 (2009).
  • Campbell EJ, Campbell MA, Boudkedes SS, Owen CA. Quantum proteolysis by neutrophils: implications for pulmonary emphysema in α(1)-antitrypsin deficiency. J. Clin. Invest.104, 337–344 (1999).
  • Rennard SI, Togo S, Holz O. Cigarette smoke inhibits alveolar repair: a mechanism for the development of emphysema. Proc. Am. Thorac. Soc.3, 703–708 (2006).
  • Wright JL, Cosio M, Churg A. Animal models of chronic obstructive pulmonary disease. Am. J. Physiol.295, L1–L5 (2008).
  • Yoshida T, Tuder RM. Pathobiology of chronic obstructive pulmonary disease. Physiol. Rev.87, 1047–1082 (2007).
  • Churg A, Zhou S, Preobrazhenska O, Tai H, Wang R, Wright JL. Expression of profibrotic mediators in small airways vs parenchyma after cigarette smoke exposure. Am. J. Respir. Cell Mol. Biol.40, 268–276 (2009).
  • Kohansal R, Martinez-Camblor P, Agusti A, Buist AS, Mannino DM, Soriano JB. The natural history of chronic airflow obstruction revisited. Am. J. Respir. Crit. Care Med.180, 3–10 (2009).
  • Hogg JC, Chu F, Utokaparch S et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N. Engl. J. Med.350, 2645–2653 (2004).
  • Hogg JC, McDonough JE, Gosselink JV, Hayashi S. What drives the peripheral lung-remodeling process in chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc.6, 668–672 (2009).
  • Wright JL, Postma DS, Kerstjens HAM, Timens W, Whittaker P, Churg A. Airway remodeling in the smoke exposed guinea pig model. Inhal. Toxicol.19, 915–923 (2007).
  • Berge S, Wedzicha JA. COPD exacerbations: definitions and classifications. Eur. Respir. J.41, 46s–53s (2003).
  • Bracke KR, D’hulst AI, Maes T et al. Cigarette smoke-induced pulmonary inflammation, but not airway remodelling, is attenuated in chemokine receptor 5-deficient mice. Clin. Exp. Allergy37, 1467–1479 (2007).
  • Lee J-H, Lee D-S, Kim E-K et al. Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs. Am. J. Respir. Crit. Care Med.172, 987–993 (2005).
  • Ou X-M, Wen F-Q, Uhal BD et al. Simvastatin attenuates experimental small airway remodelling in rats. Respirology14, 734–745 (2009).
  • Wright JL, Zhou S, Preobrazhenska O et al. Statin reverses smoke-induced pulmonary hypertension and prevents emphysema but not airway remodeling. Am. J. Respir. Crit. Care Med.(2010) (In press).
  • Traver GA, Cline MG, Burrows B. Predictors of mortality in chronic obstructive pulmonary disease. Am. Rev. Respir. Dis.119, 895–902 (1979).
  • Elwing J, Panos RJ. Pulmonary hypertension associated with COPD. Int. J. COPD3, 55–70 (2008).
  • Naeije R, Barbera JA. Pulmonary hypertension associated with COPD. Crit. Care5, 286–289 (2001).
  • Hida W, Tun Y, Kikuchi Y, Okabe S, Shirato K. Pulmonary hypertension in patients with chronic obstructive pulmonary disease: recent advances in pathophysiology and management. Respirology7, 3–13 (2002).
  • Hoeper MM. Treating pulmonary hypertension in COPD: where do we start. Eur. Respir. J.32, 541–542 (2008).
  • Barbera JA, Blanco I. Pulmonary hypertension in patients with chronic obstructive pulmonary disease. Drugs69, 1153–1171 (2009).
  • Wright JL, Lawson L, Pare PD et al. The structure and function of the pulmonary vasculature in mild chronic obstructive pulmonary disease. Am. Rev. Respir. Dis.128, 702–707 (1983).
  • 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.130, 716–721 (1984).
  • Wright JL, Petty TL, Thurlbeck WM. Analysis of the structure of the muscular pulmonary arteries in patients with pulmonary hypertension and COPD: National Institutes of Health Nocturnal Oxygen Therapy Trial. Lung170, 109–124 (1992).
  • Barbera JA, Peinado VI, Santos S. Pulmonary hypertension in chronic obstructive pulmonary disease. Eur. Respir. J.21, 892–905 (2003).
  • Kubo K, Ge R-L, Koizumi T et al. Pulmonary artery remodeling modifies pulmonary hypertension during exercise in severe emphysema. Respir. Physiol.120, 71–79 (2000).
  • Haniuda M, Kubo K, Fijimoto K et al. Effects of pulmonary artery remodeling on pulmonary circulation after lung volume reduction surgery. Thorac. Cardiovasc. Surg.51, 154–158 (2003).
  • 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.122, 273–278 (1980).
  • Kiowski W, Linder L, Stoschitzky K et al. Diminished vascular response to inhibition of endothelium-derived nitric oxide and enhanced vasoconstriction to exogenously administered endothelin-1 in clinically healthy smokers. Circulation90, 27–34 (1994).
  • Dinh-Xuan AT, Higenbottam TW, Clelland CA et al. Impairment of endothelium-dependent pulmonary-artery relaxation in chronic obstructive lung disease. N. Engl. J. Med.324, 1539–1547 (1991).
  • Dinh-Xuan AT, Pepke-Zaba J, Butt AY, Cremona G, Higenbottam TW. Impairment of pulmonary-artery endothelium-dependent relaxation in chronic obstructive lung disease is not due to dysfunction of endothelial cell membrane receptors nor to L-arginine deficiency. Br. J. Pharmacol.109, 587–591 (1993).
  • Nadziejko C, Fang K, Bravo A, Gordon T. Susceptibility to pulmonary hypertension in inbred strains of mice exposed to cigarette smoke. J. Appl. Physiol.102, 1780–1785 (2007).
  • Wright JL, Churg A. Effect of long-term cigarette smoke exposure on pulmonary vascular structure and function in the guinea pig. Exp. Lung Res.17, 997–1009 (1991).
  • 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.82, 1644–1653 (1997).
  • Wright JL. The relationship of increased pulmonary artery pressure and airflow obstruction to emphysema. J. Appl. Physiol.74, 1320–1324 (1993).
  • Wright JL, Tai H, Churg A. Vasoactive mediators and pulmonary hypertension after cigarette smoke exposure in the guinea pig. J. Appl. Physiol.100, 672–678 (2006).
  • Ferrer E, Peinado VI, Diez M et al. Effects of cigarette smoke on endothelial function of pulmonary arteries in the guinea pig. Respir. Res.10, 76–87 (2009).
  • Wright JL, Tai H, Churg A. Cigarette smoke induces persisting increases of vasoactive mediators in pulmonary arteries. Am. J. Respir. Cell Mol. Biol.31, 501–509 (2004).
  • Wright JL, Sun J-P, Churg A. Glutathione levels play a role in cigarette smoke induced cell proliferation in the rat lung. Inhal. Toxicol.10, 969–994 (1998).
  • Wright JL, Jeng AY, Battistini B. Effect of ECE and NEP inhibition on cigarette smoke-induced cell proliferation in the rat lung. Inhal. Toxicol.13, 497–511 (2001).
  • Dadmanesh F, Wright JL. Endothelin-A receptor antagonist BQ-610 blocks ciagrette smoke-induced mitogenesis in rat airways and vessels. Am. J. Physiol.272, L614–L618 (1997).
  • Wright JL, Farmer SG, Churg A. A neutrophil elastase inhibitor reduces cigarette smoke-induced remodelling of lung vessels. Eur. Respir. J.22, 77–81 (2003).
  • Churg A, Wang R, Wang X, Onnervik P-O, Thim K, Wright JL. An MMP-9/-12 inhibitor prevents smoke-induced emphysema and small airway remodeling in guinea pigs. Thorax62, 706–713 (2007).
  • De Cunto G, Cardini S, Cirino G, Geppetti P, Lungarella G, Lucattelli M. Pulmonary hypertension in smoking mice over-expressing protease-activated receptor-2. Eur. Respir. J. DOI: 10.1183/09031936.00060210 (2010) (Epub ahead of print).
  • Wright JL, Churg A. Short-term exposure to cigarette smoke induces endothelial dysfunction in small intrapulmonary arteries: analysis using guinea pig precision cut lung slices. J. Appl. Physiol.104, 1462–1469 (2008).
  • Milot J, Mechi B, Rad MTS et al. The effect of smoking cessation and steroid treatment on emphyseam in guinea pigs. Resp. Med.101, 2327–2335 (2007).
  • Wright JL, Churg A. Smoking cessation decreases the number of metaplastic secretory cells in the small airways of the guinea pig. Inhal. Toxicol.14, 101–107 (2002).
  • Wright JL, Sun J-P. The effect of smoking cessation on pulmonary and cardiovascular function and structure. J. Appl. Physiol.76, 2163–2168 (1994).
  • March TH, Wilder JA, Esparza DC et al. Modulators of cigarette smoke-induced pulmonary emphysema in A/J mice. Toxicol. Sci.92, 545–559 (2006).
  • Seagrave JC, Barr EB, March TH. Effects of cigarette smoke exposure and cessation on inflammatory cells and matrix metalloproteinase activity in mice. Exp. Lung Res.30, 1–15 (2004).
  • Motz GT, Eppert BL, Sun G et al. Persistence of lung CD8 T cell oligoclonal expansions upon smoking cessation in a mouse model of cigarette smoke-induced emphysema. J. Immunol.181, 8036–8043 (2008).
  • Braber S, Henricks PAJ, Nijkamp FP, Kraneveld AD, Folkerts G. Inflammatory changes in the airways of mice caused by cigarette smoke exposure are only partially reversed after smoking cessation. Respir. Res.11, 99–111 (2010).
  • Retamales I, Elliott WM, Meshi B et al. Amplification of inflammation in emphysema and its association with latent adenoviral infection. Am. Rev. Respir. Dis.164, 469–473 (2001)
  • Mullen 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. Thorax42, 843–848 (1987).
  • Wright JL, Lawson LM, Kennedy S, Wiggs B, Hogg JC. The detection of small airways disease. Am. Rev. Respir. Dis.129, 989–994 (1984).
  • Voynow JA, Gendler SJ, Rose MC. Regulation of mucin genes in chronic inflammatory airway diseases. Am. J. Respir. Cell Mol. Biol.34, 661–665 (2006).
  • Goco RV, Kress MB, Brantigan OC. Comparison of mucus glands in the tracheobronchial tree of man and animals. Ann. NY Acad. Sci.106, 555–571 (1963).
  • Walker D, Wilton LV, Binns R. Inhalation toxicity studies on cigarette smoke (VII) 6-week comparative experiments using modified flue-cured cigarettes: histopathology of the conducting airways. Toxicology10, 241–259 (1978).
  • Jones R, Bolduc P, Reid LM. Goblet cell glycoprotein and tracheal gland hypertrophy in rat airways: the effect of tobacco smoke with and without the antiinflammatory agent phenylmethyloxadiozole. Br. J. Exp. Pathol.54, 229–239 (1973).
  • Hayashi M, Sornberger GC, Huber GL. Morphometric analysis of tracheal gland secretion and hypertrophy in male and female rats after experimental exposure to tobacco smoke. Am. Rev. Respir. Dis.119, 67–73 (1979).
  • Rose MC, Voynow JA. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol. Rev.86, 245–278 (2006).
  • Rose MC, Nickola TJ, Voynow JA. Airway mucus obstruction: mucin glycoproteins, MUC gene regulation and goblet cell hyperplasia. Am. J. Respir. Cell Mol. Biol.25, 533–537 (2001).
  • Chorley BN, Crews AL, Li Y, Adler κB, Minnnicozzi M, Martin LD. Differential MUC2 and MUC5AC secretion by stimulated guinea pig tracheal epithelial cells in vivo. Respir. Res.7, 35–48 (2006).
  • Park SS, Kikkawa Y, Goldring IP et al. An animal model of cigarette smoking in beagle dogs. Am. Rev. Respir. Dis.115, 971–979 (1977).
  • Hayashi M, Sornberger GC, Huber GL. Differential response in the male and female tracheal epithelium following chronic tobacco smoke inhalation. Chest4, 515–518 (1978).
  • Jones R, Dolduc P, Reid L. Protection of rat bronchial epithelium against tobacco smoke. Br. Med. J.2, 142–144 (1972).
  • Lamb D, Reid L. Goblet cell increase in rat bronchial epithelium after expsoure to cigarette and cigar tobacco smoke. Br. Med. J.1, 33–35 (2001).
  • Rogers DF, Jeffery PK. Inhibition by oral N-acteylcysteine of cigarette smoke-induced ‘bronchitis’ in the rat. Exp. Lung Res.10, 267–283 (1986).
  • Bernfeld P, Homburger F, Soto E, Pai KJ. Cigarette smoke inhalation studies in inbred Syrian Golden hamsters. J. Natl Cancer Inst.63, 675–689 (1979).
  • 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.18, 105–114 (1992).
  • Bartalesi B, Cavarra E, Fineschi S et al. Different lung responses to cigarette smoke in two strains of mice sensitive to oxidants. Eur. Respir. J.25, 15–22 (2005).
  • Haswell LE, Hewitt K, Thorne D, Richter A, Gaca MD. Cigarette smoke total particulate matter increases mucous secreting cell numbers in vitro: a potential model of goblet cell hyperplasia. Toxicol. In Vitro24, 981–987 (2010).
  • Deshmukh HS, Case LM, Wesselkamper SC et al. Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation. Am. J. Respir. Crit. Care Med.171, 305–314 (2005).
  • Fischer BM, Voynow JA. Neutrophil elastase induces MUC5AC gene expression in airway epithelium via a pathway involving reactive oxygen species. Am. J. Respir. Cell Mol. Biol.26, 447–452 (2002).
  • Voynow JA, Fischer BM, Malarkey DE et al. Neutrophil elastase induces mucus cell metaplasia in mouse lung. Am. J. Physiol.287, L1293–L1302 (2004).
  • Baginski TK, Dabbagh K, Satjawatcharaphong C, Swinney DC. Cigarette smoke syndergistically enhances respiratroy mucin induction by proinflammatory stimuli. Am. J. Respir. Cell Mol. Biol.35, 165–174 (2006).
  • Levine SJ, Larivée P, Logun C, Angus CW, Ognibene FP, Shelhamer JH. Tumor necrosis factor-α induces mucin hypersecretion and MUC-2 gene expression by human airway epithelial cells. Am. J. Respir. Cell Mol. Biol.12, 196–204 (1995).
  • Takeyama K, Jung B, Shim JJ et al. Activation of epidermal growth factor receptors is responsible for mucin synthesis induced by cigarette smoke. Am. J. Physiol.280, L165–L172 (2002).
  • Shao MXG, Nakanaga T, Nadel JA. Cigarette smoke induces MUC5AC mucin overproduction via tumor necrosis factor-α-converting enzyme in human airway epithelial (NCI-H292) cells. Am. J. Physiol.287, L420–L427 (2004).
  • Leikauf GD, Borchers MT, Prows DR, Simpson LG. Mucin apoprotein expression in COPD. Chest121, 166S–182S (2002).
  • Lee SY, Kang EJ, Hur GY et al. The inhibitory effects of rebamipide on cigarette smoke-induced airway mucin production. Respir. Med.100, 503–511 (2005).
  • Komori M, Inoue H, Matsumoto K et al. PAF mediates cigarette smoke-induced goblet cell metaplasia in guinea pig airways. Am. J. Physiol.280, L436–L441 (2001).
  • Celli BR, Barnes PJ. Exacerbations of chronic obstructive pulmonary disease. Eur. Respir. J.29, 1224–1238 (2007).
  • Mallia P, Johnston SL. Mechanisms and experimental models of chronic obstructive pulmonary disease exacerbations. Proc. Am. Thorac. Soc.2, 361–366 (2005).
  • Effing TW, Kerstjens HAM, Monninkhof EM et al. Definitions of exacerbations. Chest136, 918–923 (2009).
  • Sapey E, Stockley RA. COPD exacerbations 2: aetiology. Thorax61, 250–258 (2006).
  • Wedzicha JA. Role of viruses in exacerbations of chronic obstructive pulmonary disease. Proc. Am. Thorac. Soc.17, 115–120 (2004).
  • Papi A, Contoli M, Gaetano C, Mallia P, Johnston SL. Models of infection and exacerbations in COPD. Curr. Opin. Pharm.7, 1–7 (2007).
  • Hurst JR, Perera WR, Wilkinson TMA, Donaldson GC, Wedzicha JA. Systemic and upper and lower airway inflammation at exacerbation of chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.173, 71–78 (2006).
  • Tsoumakidou M, Demedts IK, Brusselle GG, Jeffery PK. Dendritic cells in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med.177, 1180–1186 (2008).
  • Lee KM, Renne RA, Harbo SJ, Clark ML, Johnson RE, Gideon KM. 3-week inhalation exposure to cigarette smoke and/or lipopolysaccharide in AKR/1 mice. Inhal. Toxicol.19, 23–35 (2007).
  • Meng QR, Gideon KM, Harbo SJ et al. Gene expression profiling in lung tissues from mice exposed to cigarette smoke, lipopolysaccharide, or smoke plus lipopolysaccharide by inhalation. Inhal. Toxicol.18, 555–568 (2006).
  • Vernooy JHJ, Dentener MA, van Suylen RJ, Buurman WA, Wouters EFM. Long-term intratracheal lipopolysaccharide exposure in mice results in chronic lung inflammation and persistent pathology. Am. J. Respir. Cell Mol. Biol.26, 152–159 (2002).
  • Koyama J, Ahmed K, Zhao J et al. Strain-specific pulmonary defense achieved after repeated airway immunization with non-typeable Haemophilus influenzae in a mouse model. Tohoku J. Exp. Med.211, 63–74 (2007).
  • Gaschler GF, Bauer CMT, Zavitz CCJ, Stampfli MR. Animal models of chronic obstructive pulmonary disease exacerbations. Contrib. Microbiol.14, 126–141 (2007).
  • Stampfli MR, Anderson GP. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol.9, 377–384 (2009).
  • Robbins CS, Franco F, Mouded M, Cernadas M, Shapiro SD. Cigarette smoke exposure impairs dendritic cell maturation and T cell proliferation in thoracic lymph nodes of mice. J. Immunol.180, 6623–6628 (2008).
  • Motz GT, Eppert BL, Wortham BW et al. Chronic cigarette smoke exposure primes NK cell activation in a mouse model of chronic obstructive pulmonary disease. J. Immunol.184, 4460–4469 (2010).
  • Robbins CS, Dawe DE, Goncharova SI et al. Cigarette smoke decreases pulmonary dendritic cells and impacts antiviral immune responsiveness. Am. J. Respir. Cell Mol. Biol.30, 202–211 (2004).
  • Kang M-J, Lee CG, Lee J-Y et al. Cigarette smoke selectively enhances viral PAMP and virus-induced pulmonary innate immune and remodeling responses in mice. J. Clin. Invest.118, 2771–2784 (2008).
  • Gaschler GJ, Zavitz CCJ, Bauer CMT, Stampfli MR. Mechanisms of clearance of nontypeable Haemophilus influenzae from cigarette smoke-exposed mouse lungs. Eur. Respir. J.DOI:10.1183/09031936.00113909 (2010) (Epub ahead of print).
  • Phipps JC, Aronoff DM, Curtis JL, Goel D, O’Brien E, Mancuso P. Cigarette smoke exposure impairs pulmonary bacterial clearance and alveolar macrophage complement-mediated phagocytosis of Streptococcus pneumoniae. Infect. Immun.78, 1214–1230 (2010).
  • Churg A, Zhou S, Wang X, Wang R, Wright JL. The role of interleukin-1β in murine cigarette smoke-induced emphysema and small airway remodeling. Am. J. Respir. Cell Mol. Biol.40, 482–490 (2009).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.