Nontypeable haemophilus influenzae induces sustained lung oxidative stress and protease expression

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  King, Paul T ^a   Sharma, Roleen ^a   O'Sullivan, Kim ^a   Selemidis, Stavros ^b   Lim, Steven ^a   Radhakrishna, Naghmeh ^a   Lo, Camden ^b   Prasad, Jyotika ^a   Callaghan, Judy ^b   McLaughlin, Peter ^a   Farmer, Michael ^a   Steinfort, Daniel ^a   Jennings, Barton ^a   Ngui, James ^a   Broughton, Bradley R S ^b   Thomas, Belinda ^a,c   Essilfie, Ama Tawiah ^d   Hickey, Michael ^a   Holmes, Peter W ^a   Hansbro, Philip ^d   Bardin, Philip G ^a,c   Holdsworth, Stephen R ^a   more..

^a MONASH MEDICAL CENTRE   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; DEOXYRIBONUCLEASE; MACROPHAGE ELASTASE; PROTEINASE; REACTIVE OXYGEN METABOLITE;

ADULT; AMINO ACID SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; ENZYME SYNTHESIS; EXTRACELLULAR TRAP; FEMALE; FIBROBLAST; HAEMOPHILUS INFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; LUNG ALVEOLUS EPITHELIUM; LUNG ALVEOLUS MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; NONTYPEABLE HAEMOPHILUS INFLUENZAE; OXIDATIVE STRESS; PHAGOCYTE; PNEUMONIA; PROTEIN EXPRESSION; ANIMAL; BACTERIUM IDENTIFICATION; BAGG ALBINO MOUSE; CELL POLARITY; ENZYMOLOGY; EXTRACELLULAR SPACE; HAEMOPHILUS INFLUENZAE; LUNG; LUNG LAVAGE; MACROPHAGE; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; MUS;

ANIMALS; BACTERIAL TYPING TECHNIQUES; BRONCHOALVEOLAR LAVAGE; CELL POLARITY; DEOXYRIBONUCLEASES; ENDOPEPTIDASES; EXTRACELLULAR SPACE; EXTRACELLULAR TRAPS; FEMALE; HAEMOPHILUS INFLUENZAE; HUMANS; LUNG; MACROPHAGES; MALE; MICE, INBRED BALB C; MIDDLE AGED; OXIDATIVE STRESS; PHAGOCYTES; REACTIVE OXYGEN SPECIES;

EID: 84925832868     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120371     Document Type: Article

References (36)

1. Murphy TF. Haemophilus infections. In: Braunwald F, Kaspar, Hauser, Longo, Jameson, editor. Harrisons Principles of Internal Medicine. 16 th ed. New York: McGraw Hill; 2005. p. 824-829.
2. Moller LV, Timens W, van der Bij W, Kooi K, de Wever B, Dankert J, et al. Haemophilus influenzae in lung explants of patients with end-stage pulmonary disease. Am J Respir Crit Care Med 1998; 157: 950-956. PMID: 9517616
3. Dromann D, Rupp J, Rohmann K, Osbahr S, Ulmer AJ, Marwitz S, et al. The TGF-beta-pseudoreceptor BAMBI is strongly expressed in COPD lungs and regulated by nontypeable Haemophilus influenzae. Respir Res. 2010; 11: 67. doi: 10.1186/1465-9921-11-67 PMID: 20513241
4. Eldika N, Sethi S. Role of nontypeable Haemophilus influenzae in exacerbations and progression of chronic obstructive pulmonary disease. Curr Opin Pulm Med. 2006; 12: 118-124. PMID: 16456381
5. Bolduc GR, Bouchet V, Jiang RZ, Geisselsoder J, Truong-Bolduc QC, Rice PA, et al. Variability of outer membrane protein P1 and its evaluation as a vaccine candidate against experimental otitis media due to nontypeable Haemophilus influenzae: an unambiguous, multifaceted approach. Infect Immunity. 2000; 68: 4505-4517. PMID: 10899849
6. Patel IS, Seemungal TA, Wilks M, Lloyd-Owen SJ, Donaldson GC, Wedzicha JA. Relationship between bacterial colonisation and the frequency, character, and severity of COPD exacerbations. Thorax. 2002; 57: 759-764. PMID: 12200518
7. Sethi S, Sethi R, Eschberger K, Lobbins P, Cai X, Grant BJ, et al. Airway bacterial concentrations and exacerbations of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2007; 176: 356-361. PMID: 17478618
8. Cosio MG, Saetta M, Agusti A. Immunologic aspects of chronic obstructive pulmonary disease. N Engl J Med. 2009; 360(23): 2445-2454. doi: 10.1056/NEJMra0804752 PMID: 19494220
9. 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: 666-675. doi: 10.1164/rccm.200808-1306OC PMID: 19179487
10. Barnes PJ. New anti-inflammatory targets for chronic obstructive pulmonary disease. Nat Rev Drug Discov. 2013; 12: 543-559. PMID: 23977698
11. Tuder RM, Petrache I. Pathogenesis of chronic obstructive pulmonary disease. J Clin Invest. 2012; 122: 2749-2755. doi: 10.1172/JCI60324 PMID: 22850885
12. Faner R, Rojas M, Macnee W, Agusti A. Abnormal lung aging in chronic obstructive pulmonary disease and idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2012; 186: 306-313. doi: 10.1164/rccm. 201202-0282PP PMID: 22582162
13. Rahman I, MacNee W. Antioxidant pharmacological therapies for COPD. Curr Opin Pharmacol. 2012; 12: 256-265. doi: 10.1016/j.coph.2012.01.015 PMID: 22349417
14. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science. 2004; 303: 1532-1535. PMID: 15001782
15. Cheng OZ, Palaniyar N. NET balancing: a problem in inflammatory lung diseases. Frontiers in immunology. 2013; 4: 1. doi: 10.3389/fimmu.2013.00001 PMID: 23355837
16. King PT, Lim S, Pick A, Ngui J, Prodanovic Z, Downey W, et al. Lung T-cell responses to nontypeable Haemophilus influenzae in patients with chronic obstructive pulmonary disease. J Allergy Clin Immunol. 2013; 131: 1314-1321. doi: 10.1016/j.jaci.2012.09.030 PMID: 23142009
17. Aaron SD, Angel JB, Lunau M, Wright K, Fex C, Le Saux N, et al. Granulocyte inflammatory markers and airway infection during acute exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2001; 163: 349-355. PMID: 11179105
18. Barcelo B, Pons J, Fuster A, Sauleda J, Noguera A, Ferrer JM, et al. Intracellular cytokine profile of T lymphocytes in patients with chronic obstructive pulmonary disease. Clin Exper Immunol. 2006; 145: 474-479. PMID: 16907916
19. Hodge S, Matthews G, Mukaro V, Ahern J, Shivam A, Hodge G, et al. Cigarette smoke-induced changes to alveolar macrophage phenotype and function are improved by treatment with procysteine. Am J Respir Cell Mol Biol. 2011; 44: 673-681. doi: 10.1165/rcmb.2009-0459OC PMID: 20595463
20. Vlahos R, Stambas J, Bozinovski S, Broughton BR, Drummond GR, Selemidis S. Inhibition of Nox2 oxidase activity ameliorates influenza A virus-induced lung inflammation. PLoS Pathog. 2011; 7: e1001271. doi: 10.1371/journal.ppat.1001271 PMID: 21304882
21. Essilfie AT, Simpson JL, Horvat JC, Preston JA, Dunkley ML, Foster PS, et al. Haemophilus influenzae infection drives IL-17-mediated neutrophilic allergic airways disease. PLoS Pathog. 2011; 7: e1002244. doi: 10.1371/journal.ppat.1002244 PMID: 21998577
22. Drummond GR, Selemidis S, Griendling KK, Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat Rev Drug Discov. 2011; 10: 453-471. doi: 10.1038/ nrd3403 PMID: 21629295
23. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nature reviews Immunology. 2011; 11: 723-737. doi: 10.1038/nri3073 PMID: 21997792
24. Wong KW, Jacobs WR Jr. Mycobacterium tuberculosis exploits human interferon gamma to stimulate macrophage extracellular trap formation and necrosis. J Infect Dis. 2013; 208: 109-119. doi: 10.1093/ infdis/jit097 PMID: 23475311
25. Chaudhuri R, McSharry C, Brady J, Donnelly I, Grierson C, McGuinness S, et al. Sputum matrix metal-loproteinase-12 in patients with chronic obstructive pulmonary disease and asthma: relationship to disease severity. J Allergy Clin Immunol. 2012; 129: 655-663. doi: 10.1016/j.jaci.2011.12.996 PMID: 22305682
26. Keely S, Talley NJ, Hansbro PM. Pulmonary-intestinal cross-talk in mucosal inflammatory disease. Mucosal Immunol. 2012; 5: 7-18. doi: 10.1038/mi.2011.55 PMID: 22089028
27. Konstan MW, Ratjen F. Effect of dornase alfa on inflammation and lung function: potential role in the early treatment of cystic fibrosis. J Cystic Fibrosis. 2012; 11: 78-83.
28. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Nat Acad Sci. 2010; 107: 9813-9818. doi: 10.1073/pnas.0909927107 PMID: 20439745
29. Naylor EJ, Bakstad D, Biffen M, Thong B, Calverley P, Scott S, et al. Haemophilus influenzae induces neutrophil necrosis: a role in chronic obstructive pulmonary disease? Am J Respir Cell Mol Biol. 2007; 37: 135-143. PMID: 17363778
30. Harrison A, Bakaletz LO, Munson RS Jr. Haemophilus influenzae and oxidative stress. Frontiers Cell Infect Microbiol. 2012; 2: 40. doi: 10.3389/fcimb.2012.00040 PMID: 22919631
31. Shapiro SD. End-stage chronic obstructive pulmonary disease: the cigarette is burned out but inflammation rages on. Am J Respir Crit Care Med. 2001; 164: 339-340. PMID: 11500330
32. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet. 2004; 364: 709-721. PMID: 15325838
33. Wong C, Jones S. Oxidative stress and macrolides in bronchiectasis-exhaling few clues. Respirology. 2013; 18: 1037-1038. doi: 10.1111/resp.12161 PMID: 23890203
34. Hector A, Griese M, Hartl D. Oxidative stress in cystic fibrosis lung disease: an early event, but worth targeting? Eur Respir J. 2014; 44: 17-19. doi: 10.1183/09031936.00038114 PMID: 24982050
35. Juneau RA, Pang B, Weimer KE, Armbruster CE, Swords WE. Nontypeable Haemophilus influenzae initiates formation of neutrophil extracellular traps. Infect Immunity. 2011; 79: 431-438. doi: 10.1128/ IAI.00660-10 PMID: 20956567
36. O'Donnell AE, Barker AF, Ilowite JS, Fick RB. Treatment of idiopathic bronchiectasis with aerosolized recombinant human DNase I. rhDNase Study Group. Chest. 1998; 113: 1329-1334. PMID: 9596315