Cigarette smoke-promoted acquisition of bacterial pathogens in the upper respiratory tract leads to enhanced inflammation in mice

Respiratory Research

Volumn 16, Issue 1, 2015, Pages

  Voss, Meike ^a   Wonnenberg, Bodo ^a   Honecker, Anja ^a   Kamyschnikow, Andreas ^a   Herr, Christian ^a   Bischoff, Markus ^a   Tschernig, Thomas ^a   Bals, Robert ^a   Beisswenger, Christoph ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Bacterial colonization; Cigarette smoke; COPD; Inflammation

Indexed keywords

CHEMOATTRACTANT; CIGARETTE SMOKE; GELATINASE A; INTERLEUKIN 6; RANTES; AUTACOID; CYTOKINE; PASSIVE SMOKING; SMOKE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL TRANSLOCATION; BLOOD; CONTROLLED STUDY; FEMALE; GRANULOCYTE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATORY CELL; LONG TERM EXPOSURE; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; LUNG PARENCHYMA; MONOCYTE; MOUSE; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; PHAGOCYTOSIS; REAL TIME POLYMERASE CHAIN REACTION; RECURRENT INFECTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS PNEUMONIAE; UPPER RESPIRATORY TRACT; UPPER RESPIRATORY TRACT INFECTION; ADVERSE EFFECTS; ANIMAL; BACTERIAL PNEUMONIA; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; DISEASE MODEL; EXPOSURE; GENE EXPRESSION REGULATION; GENETICS; HAEMOPHILUS INFECTION; HAEMOPHILUS INFLUENZAE; IMMUNOLOGY; LUNG; METABOLISM; MICROBIOLOGY; PASSIVE SMOKING; PATHOGENICITY; SMOKE; STREPTOCOCCUS PNEUMONIA; TIME FACTOR;

ANIMALS; BACTERIAL TRANSLOCATION; BRONCHOALVEOLAR LAVAGE FLUID; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; GRANULOCYTES; HAEMOPHILUS INFECTIONS; HAEMOPHILUS INFLUENZAE; INFLAMMATION MEDIATORS; INHALATION EXPOSURE; LUNG; MICE, INBRED C57BL; MONOCYTES; PHAGOCYTOSIS; PNEUMONIA, BACTERIAL; PNEUMONIA, PNEUMOCOCCAL; SMOKE; STREPTOCOCCUS PNEUMONIAE; TIME FACTORS; TOBACCO SMOKE POLLUTION;

EID: 84927521399     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/s12931-015-0204-8     Document Type: Article

References (46)

1. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 2006;3:e442.
2. Sethi S. Infection as a comorbidity of COPD. Eur Respir J. 2010;35:1209-15.
3. Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl JMed. 2008;359:2355-65.
4. Garmendia J, Morey P, Bengoechea JA. Impact of cigarette smoke exposure on host-bacterial pathogen interactions. Eur Respir J. 2012;39:467-77.
5. Moghaddam SJ, Ochoa CE, Sethi S, Dickey BF. Nontypeable Haemophilus influenzae in chronic obstructive pulmonary disease and lung cancer. Int J Chron Obstruct Pulmon Dis. 2011;6:113-23.
6. Sethi S, Murphy TF. Bacterial infection in chronic obstructive pulmonary disease in 2000: a state-of-the-art review. Clin Microbiol Rev. 2001;14:336-63.
7. Shuto T, Xu H, Wang B, Han J, Kai H, Gu XX, et al. Activation of NF-kappa B by nontypeable Hemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKK alpha /beta-I kappa B alpha and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA. 2001;98:8774-9.
8. Veeramachaneni SB, Sethi S. Pathogenesis of bacterial exacerbations of COPD. COPD. 2006;3:109-15.
9. Herr C, Beisswenger C, Hess C, Kandler K, Suttorp N, Welte T, et al. Suppression of pulmonary innate host defence in smokers. Thorax. 2009;64:144-9.
10. Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm Res. 2008;57:497-503.
11. Charlson ES, Chen J, Custers-Allen R, Bittinger K, Li H, Sinha R, et al. Disordered microbial communities in the upper respiratory tract of cigarette smokers. PLoS One. 2010;5:e15216.
12. Brook I, Gober AE. Recovery of potential pathogens and interfering bacteria in the nasopharynx of smokers and nonsmokers. Chest. 2005;127:2072-5.
13. Brook I, Gober AE. Recovery of potential pathogens and interfering bacteria in the nasopharynx of otitis media-prone children and their smoking and nonsmoking parents. Arch Otolaryngol Head Neck Surg. 2005;131:509-12.
14. Greenberg D, Givon-Lavi N, Broides A, Blancovich I, Peled N, Dagan R. The contribution of smoking and exposure to tobacco smoke to Streptococcus pneumoniae and Haemophilus influenzae carriage in children and their mothers. Clin Infect Dis. 2006;42:897-903.
15. Zambon JJ, Grossi SG, Machtei EE, Ho AW, Dunford R, Genco RJ. Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol. 1996;67:1050-4.
16. van Winkelhoff AJ, Bosch-Tijhof CJ, Winkel EG, van der Reijden WA. Smoking affects the subgingival microflora in periodontitis. J Periodontol. 2001;72:666-71.
17. Almirall J, Bolibar I, Balanzo X, Gonzalez CA. Risk factors for community-acquired pneumonia in adults: a population-based case-control study. Eur Respir J. 1999;13:349-55.
18. Almirall J, Gonzalez CA, Balanzo X, Bolibar I. Proportion of community-acquired pneumonia cases attributable to tobacco smoking. Chest. 1999;116:375-9.
19. Nuorti JP, Butler JC, Farley MM, Harrison LH, McGeer A, Kolczak MS, et al. Cigarette smoking and invasive pneumococcal disease. Active Bacterial Core Surveillance Team. N Engl J Med. 2000;342:681-9.
20. Jones LL, Hashim A, McKeever T, Cook DG, Britton J, Leonardi-Bee J. Parental and household smoking and the increased risk of bronchitis, bronchiolitis and other lower respiratory infections in infancy: systematic review and meta-analysis. Respir Res. 2011;12:5.
21. Herr C, Han G, Li D, Tschernig T, Dinh QT, Beisswenger C, et al. Combined exposure to bacteria and cigarette smoke resembles characteristic phenotypes of human COPD in a murine disease model. Exp Toxicol Pathol. 2015;67:261-9.
22. Nelson AL, Roche AM, Gould JM, Chim K, Ratner AJ, Weiser JN. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect Immun. 2007;75:83-90.
23. Beisswenger C, Lysenko ES, Weiser JN. Early bacterial colonization induces toll-like receptor-dependent transforming growth factor beta signaling in the epithelium. Infect Immun. 2009;77:2212-20.
24. Zola TA, Lysenko ES, Weiser JN. Mucosal clearance of capsule-expressing bacteria requires both TLR and nucleotide-binding oligomerization domain 1 signaling. J Immunol. 2008;181:7909-16.
25. Li D, Beisswenger C, Herr C, Hellberg J, Han G, Zakharkina T, et al. Myeloid cell RelA/p65 promotes lung cancer proliferation through Wnt/beta-catenin signaling in murine and human tumor cells. Oncogene. 2014;33:1239-48.
26. Seiler F, Hellberg J, Lepper PM, Kamyschnikow A, Herr C, Bischoff M, et al. FOXO Transcription Factors Regulate Innate Immune Mechanisms in Respiratory Epithelial Cells. J Immunol. 2013;190:1603-13.
27. Pfeifer P, Voss M, Wonnenberg B, Hellberg J, Seiler F, Lepper PM, et al. IL-17C is a mediator of respiratory epithelial innate immune response. Am J Respir Cell Mol Biol. 2013;48:415-21.
28. McCool TL, Weiser JN. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect Immun. 2004;72:5807-13.
29. Zhang Z, Clarke TB, Weiser JN. Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice. J Clin Invest. 2009;119:1899-909.
30. Moser C, Weiner DJ, Lysenko E, Bals R, Weiser JN, Wilson JM. beta-Defensin 1 contributes to pulmonary innate immunity in mice. Infect Immun. 2002;70:3068-72.
31. Kulkarni R, Rampersaud R, Aguilar JL, Randis TM, Kreindler JL, Ratner AJ. Cigarette smoke inhibits airway epithelial cell innate immune responses to bacteria. Infect Immun. 2010;78:2146-52.
32. Chen H, Cowan MJ, Hasday JD, Vogel SN, Medvedev AE. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J Immunol. 2007;179:6097-106.
33. 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. 2010;78:1214-20.
34. Stringer KA, Tobias M, O'Neill HC, Franklin CC. Cigarette smoke extract-induced suppression of caspase-3-like activity impairs human neutrophil phagocytosis. Am J Physiol Lung Cell Mol Physiol. 2007;292:L1572-9.
35. Manzel LJ, Shi L, O'Shaughnessy PT, Thorne PS, Look DC. Inhibition by cigarette smoke of nuclear factor-kappaB-dependent response to bacteria in the airway. Am J Respir Cell Mol Biol. 2011;44:155-65.
36. 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;173:4164-70.
37. Fainstein V, Musher DM, Cate TR. Bacterial adherence to pharyngeal cells during viral infection. J Infect Dis. 1980;141:172-6.
38. El Ahmer OR, Essery SD, Saadi AT, Raza MW, Ogilvie MM, Weir DM, et al. The effect of cigarette smoke on adherence of respiratory pathogens to buccal epithelial cells. FEMS Immunol Med Microbiol. 1999;23:27-36.
39. Grigg J, Walters H, Sohal SS, Wood-Baker R, Reid DW, Xu CB, et al. Cigarette smoke and platelet-activating factor receptor dependent adhesion of Streptococcus pneumoniae to lower airway cells. Thorax. 2012;67:908-13.
40. Raman AS, Swinburne AJ, Fedullo AJ. Pneumococcal adherence to the buccal epithelial cells of cigarette smokers. Chest. 1983;83:23-7.
41. Berenson CS, Wrona CT, Grove LJ, Maloney J, Garlipp MA, Wallace PK, et al. Impaired alveolar macrophage response to Haemophilus antigens in chronic obstructive lung disease. Am J Respir Crit Care Med. 2006;174:31-40.
42. Nikota JK, Shen P, Morissette MC, Fernandes K, Roos A, Chu DK, et al. Cigarette smoke primes the pulmonary environment to IL-1alpha/CXCR-2-Dependent Nontypeable Haemophilus influenzae-Exacerbated Neutrophilia in mice. J Immunol. 2014;193:3134-45.
43. Gaschler GJ, Skrtic M, Zavitz CC, Lindahl M, Onnervik PO, Murphy TF, et al. Bacteria challenge in smoke-exposed mice exacerbates inflammation and skews the inflammatory profile. Am J Respir Crit Care Med. 2009;179:666-75.
44. Marti-Lliteras P, Regueiro V, Morey P, Hood DW, Saus C, Sauleda J, et al. Nontypeable Haemophilus influenzae clearance by alveolar macrophages is impaired by exposure to cigarette smoke. Infect Immun. 2009;77:4232-42.
45. Berenson CS, Garlipp MA, Grove LJ, Maloney J, Sethi S. Impaired phagocytosis of nontypeable Haemophilus influenzae by human alveolar macrophages in chronic obstructive pulmonary disease. J Infect Dis. 2006;194:1375-84.
46. Taylor AE, Finney-Hayward TK, Quint JK, Thomas CM, Tudhope SJ, Wedzicha JA, et al. Defective macrophage phagocytosis of bacteria in COPD. Eur Respir J. 2010;35:1039-47.