Bacteria challenge in smoke-exposed mice exacerbates inflammation and skews the inflammatory profile

American Journal of Respiratory and Critical Care Medicine

Volumn 179, Issue 8, 2009, Pages 666-675

  Gaschler, Gordon J ^a   Skrtic, Marko ^b   Zavitz, Caleb C J ^a   Lindahl, Maria ^c   Onnervik, Per Ola ^c   Murphy, Timothy F ^d   Sethi, Sanjay ^d   Stämpfli, Martin R ^b,c,e  

^a Medical Sciences Graduate Program   (Sweden)

^b Department of Pathology and Molecular Medicine   (Sweden)

^c MCMASTER UNIVERSITY   (Canada)

^d ASTRAZENECA R AND D   (Sweden)

^e UNIVERSITY AT BUFFALO   (United States)

Author keywords

Chronic obstructive pulmonary disease; Exacerbation; Mouse model; Non typeable haemophilus influenzae

Indexed keywords

CIGARETTE SMOKE; DEXAMETHASONE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1; MACROPHAGE INFLAMMATORY PROTEIN 1GAMMA; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; MONOCYTE CHEMOTACTIC PROTEIN 5; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DOSE RESPONSE; FEMALE; HAEMOPHILUS INFLUENZAE; LUNG ALVEOLUS MACROPHAGE; LUNG INJURY; MOUSE; NEUTROPHIL COUNT; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; WEIGHT REDUCTION;

ADMINISTRATION, INTRANASAL; ANIMALS; DISEASE PROGRESSION; FEMALE; HAEMOPHILUS INFLUENZAE; INFLAMMATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; TOBACCO SMOKE POLLUTION;

EID: 65249182139     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200808-1306OC     Document Type: Article

References (54)

1. Mannino DM, Buist AS. Global burden of COPD: risk factors, prevalence, and future trends. Lancet 2007;370:765-773.
2. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet 2004;364:709-721.
3. Hogg JC, Chu F, Utokaparch S, Woods R, Elliott WM, Buzatu L, Cherniack RM, Rogers RM, Sciurba FC, Coxson HO, et al. The nature of small-airway obstruction in chronic obstructive pulmonary disease. N Engl J Med 2004;350:2645-2653.
4. Barnes PJ. Immunology of asthma and chronic obstructive pulmonary disease. Nat Rev Immunol 2008;8:183-192.
5. Barnes PJ. Alveolar macrophages as orchestrators of COPD. COPD 2004;1:59-70.
6. Aaron SD, Angel JB, Lunau M, Wright K, Fex C, Le Saux N, Dales RE. Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;163:349-355.
7. Papi A, Bellettato CM, Braccioni F, Romagnoli M, Casolari P, Caramori G, Fabbri LM, Johnston SL. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med 2006;173:1114-1121.
8. Sethi S, Muscarella K, Evans N, Klingman KL, Grant BJ, Murphy TF. Airway inflammation and etiology of acute exacerbations of chronic bronchitis. Chest 2000;118:1557-1565.
9. Wedzicha JA, Seemungal TA. COPD exacerbations: defining their cause and prevention. Lancet 2007;370:786-796.
10. Sethi S, Evans N, Grant BJ, Murphy TF. New strains of bacteria and exacerbations of chronic obstructive pulmonary disease. N Engl J Med 2002;347:465-471.
11. 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.
12. Sethi S, Maloney J, Grove L, Wrona C, Berenson CS. Airway inflammation and bronchial bacterial colonization in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2006;173:991-998.
13. Bresser P, Out TA, van Alphen L, Jansen HM, Lutter R. Airway inflammation in nonobstructive and obstructive chronic bronchitis with chronic haemophilus influenzae airway infection. Comparison with noninfected patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000;162:947-952.
14. Gaschler GJ, Skrtic M, Zavitz CCJ, Stampfli MR. Cigarette smoke alters the cellular and cytokine profile following in vivo challenge with nontypeable Haemophilus influenzae in mice [abstract]. Am J Respir Crit Care Med 2008;177:A864.
15. Fernaays MM, Lesse AJ, Cai X, Murphy TF. Characterization of IgAb, a second immunoglobulin A1 protease gene in nontypeable haemo- philus influenzae. Infect Immun 2006;74:5860-5870.
16. Yi K, Sethi S, Murphy TF. Human immune response to nontypeable haemophilus influenzae in chronic bronchitis. J Infect Dis 1997;176:1247-1252.
17. Gaschler GJ, Zavitz CC, Bauer CM, Skrtic M, Lindahl M, Robbins CS, Chen B, Stampfli MR. Cigarette smoke exposure attenuates cytokine production by mouse alveolar macrophages. Am J Respir Cell Mol Biol 2008;38:218-226.
18. Wang X, Moser C, Louboutin JP, Lysenko ES, Weiner DJ, Weiser JN, Wilson JM. Toll-like receptor 4 mediates innate immune responses to haemophilus influenzae infection in mouse lung. J Immunol 2002;168:810-815.
19. Wieland CW, Florquin S, Maris NA, Hoebe K, Beutler B, Takeda K, Akira S, van der Poll T. The MyD88-dependent, but not the MyD88-independent, pathway of TLR4 signaling is important in clearing nontypeable haemophilus influenzae from the mouse lung. J Immunol 2005;175:6042-6049.
20. Holt PG. Down-regulation of immune responses in the lower respiratory tract:the role of alveolar macrophages. Clin Exp Immunol 1986;63:261-270.
21. Lapperre TS, Willems LN, Timens W, Rabe KF, Hiemstra PS, Postma DS, Sterk PJ. Small airways dysfunction and neutrophilic inflammation in bronchial biopsies and BAL in COPD. Chest 2007;131:53-59.
22. O'Donnell RA, Peebles C, Ward JA, Daraker A, Angco G, Broberg P, Pierrou S, Lund J, Holgate ST, Davies DE, et al. Relationship between peripheral airway dysfunction, airway obstruction, and neutrophilic inflammation in COPD. Thorax 2004;59:837-842.
23. Binnie V, McHugh S, Macpherson L, Borland B, Moir K, Malik K. The validation of self-reported smoking status by analysing cotinine levels in stimulated and unstimulated saliva, serum and urine. Oral Dis 2004;10:287-293.
24. de Weerd S, Thomas CM, Kuster JE, Cikot RJ, Steegers EA. Variation of serum and urine cotinine in passive and active smokers and applicability in preconceptional smoking cessation counseling. Environ Res 2002;90:119-124.
25. Churg A, Tai H, Coulthard T, Wang R, Wright JL. Cigarette smoke drives small airway remodeling by induction of growth factors in the airway wall. Am J Respir Crit Care Med 2006;174:1327-1334.
26. Guddo F, Vignola AM, Saetta M, Baraldo S, Siena L, Balestro E, Zuin R, Papi A, Maestrelli P, Fabbri LM, et al. Upregulation of basic fibroblast growth factor in smokers with chronic bronchitis. Eur Respir J 2006;27:957-963.
27. Kranenburg AR, Willems-Widyastuti A, Mooi WJ, Saxena PR, Sterk PJ, de Boer WI, Sharma HS. Chronic obstructive pulmonary disease is associated with enhanced bronchial expression of FGF-1, FGF-2, and FGFR-1. J Pathol 2005;206:28-38.
28. Burge S, Wedzicha JA. COPD exacerbations: definitions and classifications. Eur Respir J 2003;41:46s-53s.
29. Aronson MD, Weiss ST, Ben RL, Komaroff AL. Association between cigarette smoking and acute respiratory tract illness in young adults. JAMA 1982;248:181-183.
30. Seemungal TA, Donaldson GC, Bhowmik A, Jeffries DJ, Wedzicha JA. Time course and recovery of exacerbations in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2000;161:1608-1613.
31. Murphy TF, Brauer AL, Schiffmacher AT, Sethi S. Persistent colonization by haemophilus influenzae in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2004;170:266-272.
32. Naylor EJ, Bakstad D, Biffen M, Thong B, Calverley P, Scott S, Hart CA, Moots RJ, Edwards SW. Haemophilus influenzae induces neutrophil necrosis: a role in chronic obstructive pulmonary disease? Am J Respir Cell Mol Biol 2007;37:135-143.
33. Hodge S, Hodge G, Scicchitano R, Reynolds PN, Holmes M. Alveolar macrophages from subjects with chronic obstructive pulmonary disease are deficient in their ability to phagocytose apoptotic airway epithelial cells. Immunol Cell Biol 2003;81:289-296.
34. Hodge S, Hodge G, Ahern J, Jersmann H, Holmes M, Reynolds PN. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2007;37:748-755.
35. Johnston B, Burns AR, Suematsu M, Issekutz TB, Woodman RC, Kubes P. Chronic inflammation upregulates chemokine receptors and induces neutrophil migration to monocyte chemoattractant protein-1. J Clin Invest 1999;103:1269-1276.
36. Ito K, Ito M, Elliott WM, Cosio B, Caramori G, Kon OM, Barczyk A, Hayashi S, Adcock IM, Hogg JC, et al. Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 2005;352:1967-1976.
37. Thatcher TH, Maggirwar SB, Baglole CJ, Lakatos HF, Gasiewicz TA, Phipps RP, Sime PJ. Aryl hydrocarbon receptor-deficient mice develop heightened inflammatory responses to cigarette smoke and endotoxin associated with rapid loss of the nuclear factor-kappab component relb. Am J Pathol 2007;170:855-864.
38. Baglole CJ, Maggirwar SB, Gasiewicz TA, Thatcher TH, Phipps RP, Sime PJ. The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the nf-kappab family member relb. J Biol Chem 2008;283:28944-28957.
39. Natarajan S, Kim J, Remick DG. Acute pulmonary lipopolysaccharide tolerance decreases tnf-alpha without reducing neutrophil recruitment. J Immunol 2008;181:8402-8408.
40. Kasahara DI, Poynter ME, Othman Z, Hemenway D, van der Vliet A. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airways neutrophilia. J Immunol 2008;181:736-745.
41. Wheeler DS, Lahni PM, Denenberg AG, Poynter SE, Wong HR, Cook JA, Zingarelli B. Induction of endotoxin tolerance enhances bacterial clearance and survival in murine polymicrobial sepsis. Shock 2008;30:267-273.
42. Freudenberg MA, Galanos C. Induction of tolerance to lipopolysaccharide (LPS)-d-galactosamine lethality by pretreatment with lps is mediated by macrophages. Infect Immun 1988;56:1352-1357.
43. Russell RE, Culpitt SV, DeMatos C, Donnelly L, Smith M, Wiggins J, Barnes PJ. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2002;26:602-609.
44. Berenson CS, Wrona CT, Grove LJ, Maloney J, Garlipp MA, Wallace PK, Stewart CC, Sethi S. Impaired alveolar macrophage response to haemophilus antigens in chronic obstructive lung disease. Am J Respir Crit Care Med 2006;174:31-40.
45. Birrell MA, Wong S, Catley MC, Belvisi MG. Impact of tobacco-smoke on key signaling pathways in the innate immune response in lung macrophages. J Cell Physiol 2008;214:27-37.
46. Laan M, Bozinovski S, Anderson GP. Cigarette smoke inhibits lipopolysaccharide-induced production of inflammatory cytokines by suppressing the activation of activator protein-1 in bronchial epithelial cells. J Immunol 2004;173:4164-4170.
47. Burge PS, Calverley PM, Jones PW, Spencer S, Anderson JA, Maslen TK. Randomised, double blind, placebo controlled study of fluticasone propionate in patients with moderate to severe chronic obstructive pulmonary disease: the ISOLDE trial. BMJ 2000;320:1297-1303.
48. Group LHSR. Effect of inhaled triamcinolone on the decline in pulmonary function in chronic obstructive pulmonary disease. N Engl J Med 2000;343:1902-1909.
49. Calverley PM, Anderson JA, Celli B, Ferguson GT, Jenkins C, Jones PW, Yates JC, Vestbo J. Salmeterol and fluticasone propionate and survival in chronic obstructive pulmonary disease. N Engl J Med 2007;356:775-789.
50. Ernst P, Gonzalez AV, Brassard P, Suissa S. Inhaled corticosteroid use in chronic obstructive pulmonary disease and the risk of hospitalization for pneumonia. Am J Respir Crit Care Med 2007;176:162-166.
51. Kardos P, Wencker M, Glaab T, Vogelmeier C. Impact of salmeterol/fluticasone propionate versus salmeterol on exacerbations in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2007;175:144-149.
52. Satoh S, Oishi K, Iwagaki A, Senba M, Akaike T, Akiyama M, Mukaida N, Atsushima KM, Nagatake T. Dexamethasone impairs pulmonary defence against pseudomonas aeruginosa through suppressing iNOS gene expression and peroxynitrite production in mice. Clin Exp Immunol 2001;126:266-273.
53. Schleimer RP. How do steroids work? Am J Respir Crit Care Med 1996;153:S28-S30.
54. Culpitt SV, Rogers DF, Shah P, De Matos C, Russell RE, Donnelly LE, Barnes PJ. Impaired inhibition by dexamethasone of cytokine release by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2003;167:24-31.