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Immune Cell Characterization in the Lung After Acute and Chronic Cigarette Smoke Exposure in a Mouse Model of Copd

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Immune Cell Characterization in the Lung After Acute and Chronic Cigarette Smoke Exposure in a Mouse Model of Copd Institut für Experimentelle Pneumologie der Universität München Direktor: Prof. Dr. med. Oliver Eickelberg Aus dem Comprehensive Pneumology Center des Helmholtz Zentrum München Direktor: Prof. Dr. med. Oliver Eickelberg IMMUNE CELL CHARACTERIZATION IN THE LUNG AFTER ACUTE AND CHRONIC CIGARETTE SMOKE EXPOSURE IN A MOUSE MODEL OF COPD Dissertation zum Erwerb des Doktorgrades der Humanbiologie an der Medizinischen Fakultät der Ludwig-Maximilians-Universität zu München vorgelegt von Katrin Hager aus Eilenburg 2016 Mit Genehmigung der Medizinischen Fakultät der Universität München Berichterstatter: Prof. Dr. med. Oliver Eickelberg Mitberichterstatter: Prof. Dr. Albrecht Bergner Prof. Dr. Jürgen Behr Mitbetreuung durch den promovierten Mitarbeiter: Dr. Ali Önder Yildirim Dekan: Prof. Dr. med. dent. Reinhard Hickel Tag der mündlichen Prüfung: 21.10.2016 Eidesstattliche Versicherung Eidesstattliche Versicherung Ich, Katrin Hager, erkläre hiermit an Eides statt, dass ich die vorliegende Dissertation mit dem Thema „Immune cell characterization in the lung after acute and chronic cigarette smoke exposure in a mouse model of COPD“ selbständig verfasst, mich außer der angegebenen keiner weiteren Hilfsmittel bedient und alle Erkenntnisse, die aus dem Schrifttum ganz oder annähernd übernommen sind, als solche kenntlich gemacht und nach ihrer Herkunft unter Bezeichnung der Fundstelle einzeln nachgewiesen habe. Ich erkläre des Weiteren, dass die hier vorgelegte Dissertation nicht in gleicher oder in ähnlicher Form bei einer anderen Stelle zur Erlangung eines akademischen Grades eingereicht wurde. _______________________________ ________________________________ Ort, Datum Unterschrift Doktorandin/Doktorand III Table of Contents Table of Contents Table of Contents ............................................................................................................................ IV List of Abbreviations ......................................................................................................................... V List of Publications .......................................................................................................................... VII 1 Introduction ................................................................................................................................ 1 2 Zusammenfassung .................................................................................................................. 16 3 Summary ................................................................................................................................. 17 4 The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models ..................................................................................................................... 18 5 Cigarette smoke-induced iBALT mediates macrophage activation in a B cell-dependent manner in COPD ......................................................................................................................................... 34 6 Bibliography ............................................................................................................................. 52 7 Acknowledgements.................................................................................................................. 61 IV List of Abbreviations List of Abbreviations % percent IRF interferon-regulatory factor ANA antinuclear antibodies KC keratinocyte-derived cytokine BAL bronchoalveolar lavage Ko knockout CAT COPD assessment test L ligand CCL Chemokine (C-C motif) ligand Lm mean linear intercept CCR C-C chemokine receptor LF lymphoid follicle CD cluster of differentiation LPS lipopolysaccharide Chit chitotriosidase M1 classically activated Chi3l Chitinase 3-like protein macrophage CO carbon monoxide M2 alternatively activated COPD chronic obstructive pulmonary macrophage disease m3 cubic meters CS cigarette smoke MCP monocyte chemoattractant CSC cigarette smoke condensate protein CSE cigarette smoke extract mg milligram CXCL chemokine (C-X-C motif) ligand MIP macrophage inflammatory CXCR C-X-C chemokine receptor protein 2 DC dendritic cell MMP matrix metalloproteinase DMSO dimethyl sulfoxide mMRC modified Medical Research DNA desoxyribonucleic acid Council EAE experimental autoimmune µMT B cell deficient encephalomyelitis mRNA messenger RNA et al. et alii MS multiple sclerosis Fc fragment crystallisable NFκB nuclear factor 'kappa-light- FDC follicular dendritic cell chain-enhancer' of activated B- FEV forced expiratory volume cells FoxP3 forkhead box P3 NE neutrophil elastase FVC forced vital capacity NO nitric oxide G-CSF granulocyte colony-stimulating PBS phosphate buffered saline factor PCR polymerase chain reaction GM-CSF granulocyte-macrophage PE phycoerythrin colony-stimulating factor PM particulate matter GOLD global initiative for chronic R receptor obstructive lung disease RA rheumatoid arthritis h hour RNA ribonucleic acid HEV high endothelial venule ROR retinoic orphan nuclear receptor HPV human papillomavirus ROS reactive oxygen species iBALT inducible bronchus-associated SHS secondhand smoke lymphoid tissue Sv airspace wall surface to volume IBD inflammatory bowl disease ratio IFN interferon TGFβ transforming growth factor β Ig immunoglobulin Th T helper cell IL interkeukin TIMP1 TIMP metallopeptidase inhibitor iNOS inducible nitric oxide synthase 1 V List of Abbreviations TLO tertiary lymphoid organ TLR toll-like-receptor TNFα tumor necrosis factor α TPM total particulate matter Treg regulatory T cell Wt wildtype WHO World Health Organization VI List of Publications List of Publications - “Inflammaging increases susceptibility to cigarette smoke-induced COPD”, Gerrit John-Schuster, Stefanie Günther, Katrin Hager, Thomas Conlon, Oliver Eickelberg, Ali Önder Yildirm, Oncotarget, 2015 May 29. [Epub ahead of print] - “Cigarette smoke-induced iBALT mediates macrophage activation in a B cell-dependent manner in COPD”, Gerrit John-Schuster*, Katrin Hager*, Thomas Conlon, Martin Irmler, Johannes Beckers, Oliver Eickelberg, Ali Ö. Yildirim, American Journal of Physiology-Lung Cellular and Molecular Physiology, 307 L692-L706, 2014. * Authors contributed eQually to this work - “The composition of cigarette smoke determines inflammatory cell recruitment to the lung in COPD mouse models”, Gerrit John, Katrin Kohse, Jurgen Orasche, Ahmed Reda, Jurgen Schnelle-Kreis, Ralf Zimmermann, Otmar Schmid, Oliver Eickelberg, Ali Önder Yildirim, Clinical Science, 126 (3), 207-221, 2013. - “Acute cigarette smoke exposure impairs proteasome function in the lung”, Sabine H van Rijt, Ilona E Keller, Gerrit John, Katrin Kohse, Ali Önder Yildirim, Oliver Eickelberg, Silke Meiners, American Journal of Physiology-Lung Cellular and Molecular Physiology, 303 (9), L814-L823, 2012. - “All-trans retinoic acid results in irregular repair of septa and fails to inhibit proinflammatory macrophages”, Carola Seifart, Jai Prakash Muyal, Alexandra Plagens, Ali Önder Yildirim, Katrin Kohse, Veronika Grau, Sabine Sandu, Christian Reinke, Thomas Tschernig, Claus Vogelmeier, Heinz Fehrenbach, European Respiratory Journal, 38 (2), 425-439, 2011. VII 1.1 Definition of COPD 1 Introduction Definition of COPD Chronic obstructive pulmonary disease (COPD) is a major global health problem, since an estimated 64 million people suffered from COPD in 2004 (Mathers et al., 2008). In 2005 more than 3 million people died of COPD, which is eQual to 5% of all global deaths this year. The World Health Organization (WHO) ranked COPD as the third common cause of death worldwide and estimates that it will be the third by 2020 (WHO, 2008). Furthermore, COPD is one of the leading causes for hospitalization and health care incurrence (Buist et al., 2007; Gershon et al., 2010; Hall et al., 2010). COPD is a highly under-diagnosed disease and often diagnosed in a late stage. Cigarette smoking is the major cause for COPD in the industrialized countries where it accounts for 80 – 90 % of the cases (Barnes et al., 2003) . Earlier diagnosis would be important for aggressive smoking cessation efforts and by this may lead to a reduction in the burden of COPD symptoms (Tinkelman et al., 2007). In developing countries other environmental pollutants such as indoor air pollution from combustion of biomass/traditional fuels and coal are important causes of COPD (Dennis et al., 1996). Next to CS and air pollution, genetic predispositions are risk factors for developing COPD. The lack of proteinase inhibitor α-1-antitrypsin in the lung and a polymorphism of the promoter region of the pro-inflammatory cytokine tumor necrosis factor-α (TNF-α) have been associated with COPD development (WHO, 1997). Inflammatory changes are detectable in lungs of all smokers, independently of disease development, but in COPD inflammatory processes seem to be abnormal (Chung and Adcock, 2008). Deregulated inflammatory responses can subseQuently cause mucus hypersecretion (chronic bronchitis) (Sommerhoff et al., 1990) ), tissue destruction (emphysema) (Lee et al., 2007; Sullivan et al., 2005; Turato et al., 2002) as well as disruption of repair- and defense mechanisms (Rennard, 2007). Together these pathological changes lead to increased resistance to airflow in the small conducting airways, and increased compliance and reduced elastic recoil in the lungs. ConseQuences are progressive airflow limitations and air trapping, which are the hallmarks of COPD. In general, inflammatory and structural changes persist even after
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