Research Paper Volume 10, Issue 8 pp 2122—2135

A Drosophila model of cigarette smoke induced COPD identifies Nrf2 signaling as an expedient target for intervention

Ruben Prange1, , Marcus Thiedmann1, , Anita Bhandari1,5, , Neha Mishra2, , Anupam Sinha2, , Robert Häsler2, , Philipp Rosenstiel2, , Karin Uliczka3, , Christina Wagner3, , Ali Önder Yildirim4,6, , Christine Fink1,7, , Thomas Roeder1,7, ,

  • 1 Kiel University, Zoology, Department of Molecular Physiology, Kiel, Germany
  • 2 Kiel University, IKMB, Kiel, Germany
  • 3 Research Center Borstel, Invertebrate Models, Borstel, Germany
  • 4 Comprehensive Pneumology Center, Institute of Lung Biology and Disease, Helmholtz Center Munich, German Research Center for Environmental Health, Munich, Germany
  • 5 University zu Lübeck, Institute for Cardiogenetics, Lübeck, Germany
  • 6 CPC-M, Member of the German Center for Lung Research (DZL), Munich, Germany
  • 7 Airway Research Center North, Member of the German Center for Lung Research (DZL), Grosshansdorf, Germany
* Equal contribution

Received: July 25, 2018       Accepted: August 21, 2018       Published: August 27, 2018      

https://doi.org/10.18632/aging.101536
How to Cite

Copyright: © 2018 Prange et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Chronic obstructive pulmonary disease (COPD) is among the most important causes of death. Signaling systems that are relevant for tissue repair and detoxification of reactive oxygen species or xenobiotics are thought to be impaired in lungs of patients suffering from this disease. Here, we developed a simple cigarette smoke induced Drosophila model of COPD based on chronic cigarette smoke exposure that recapitulates major pathological hallmarks of the disease and thus can be used to investigate new therapeutic strategies. Chronic cigarette smoke exposure led to premature death of the animals and induced a set of phenotypes reminiscent of those seen in COPD patients, including reduced physical activity, reduced body fat, increased metabolic rate and a substantial reduction of the respiratory surface. A detailed transcriptomic analysis revealed that especially the TGF-β, Nrf2 and the JAK/STAT signaling pathways are altered by chronic cigarette smoke exposure. Based on these results, we focused on Nrf2 signaling. A pharmacological intervention study performed with oltipraz, an activator of Nrf2 signaling, increased survival of cigarette smoke exposed animals significantly. Thus, the Drosophila COPD model recapitulates many major hallmarks of COPD and it is highly useful to evaluate the potential of alternative therapeutic strategies.

Abbreviations

ARE: antioxidant response element; COPD: chronic obstructive pulmonary disease; CS: cigarette smoke; CTCF: CCCTC-binding factor; Cyp: cytochrome P; Dsrf: Drosophila serum response factor; GFP: green fluorescent protein; GO: gene ontology; GST: glutathione S transferase; GstD2/5: glutathione S transferase D2/5; IL5/6: interleukin5/6; IMD: immune deficiency; JAK/STAT: januskinase/signal transducers and activator of transcription; KEGG: Kyoto Encyclopedia of Genes and Genomes; Mad: mothers against decapentaplegic; Nrf2: nuclear factor erythroid 2–related factor 2; opa: odd paired; PBS: phosphate buffered saline; PGRP-LE-OE: peptidoglycan recognition protein LE overexpression; Prx2540: peroxiredoxin 2540; qRT-PCR: quantitative reverse transcriptase PCR; ROS: reactive oxygen species; TGF-β: transforming growth factor- β; Trl: trithorax-like; UAS: upstream activating sequence; upd2/3: unpaired2/3.