Skip to main content
Top
Published in: Respiratory Research 1/2020

01-12-2020 | Smoking and Nicotine Detoxification | Research

Cigarette smoke and electronic cigarettes differentially activate bronchial epithelial cells

Authors: Christian Herr, Konstantinos Tsitouras, Julia Niederstraßer, Christina Backes, Christoph Beisswenger, Li Dong, Loïc Guillot, Andreas Keller, Robert Bals

Published in: Respiratory Research | Issue 1/2020

Login to get access

Abstract

Background

The use of electronic cigarettes (ECIGs) is increasing, but the impact of ECIG-vapor on cellular processes like inflammation or host defense are less understood. The aim of the present study was to compare the acute effects of traditional cigarettes (TCIGs) and ECIG-exposure on host defense, inflammation, and cellular activation of cell lines and primary differentiated human airway epithelial cells (pHBE).

Methods

We exposed pHBEs and several cell lines to TCIG-smoke or ECIG-vapor. Epithelial host defense and barrier integrity were determined. The transcriptome of airway epithelial cells was compared by gene expression array analysis. Gene interaction networks were constructed and differential gene expression over all groups analyzed. The expression of several candidate genes was validated by qRT-PCR.

Results

Bacterial killing, barrier integrity and the expression of antimicrobial peptides were not affected by ECIG-vapor compared to control samples. In contrast, TCIGs negatively affected host defense and reduced barrier integrity in a significant way. Furthermore ECIG-exposure significantly induced IL-8 secretion from Calu-3 cells but had no effect on NCI-H292 or primary cells. The gene expression based on array analysis distinguished TCIG-exposed cells from ECIG and room air-exposed samples.

Conclusion

The transcriptome patterns of host defense and inflammatory genes are significantly distinct between ECIG-exposed and TCIG-treated cells. The overall effects of ECIGs on epithelial cells are less in comparison to TCIG, and ECIG-vapor does not affect host defense. Nevertheless, although acute exposure to ECIG-vapor induces inflammation, and the expression of S100 proteins, long term in vivo data is needed to evaluate the chronic effects of ECIG use.
Appendix
Available only for authorised users
Literature
3.
go back to reference Hon L: Electronic atomization cigarette. Google Patents; 2013. Hon L: Electronic atomization cigarette. Google Patents; 2013.
4.
go back to reference Gilbert HA: Smokeless non-tobacco cigarette. Google Patents; 1965. Gilbert HA: Smokeless non-tobacco cigarette. Google Patents; 1965.
5.
go back to reference Suber RL, Deskin R, Nikiforov I, Fouillet X, Coggins CR. Subchronic nose-only inhalation study of propylene glycol in Sprague-Dawley rats. Food Chem Toxicol. 1989;27:573–83.PubMedCrossRef Suber RL, Deskin R, Nikiforov I, Fouillet X, Coggins CR. Subchronic nose-only inhalation study of propylene glycol in Sprague-Dawley rats. Food Chem Toxicol. 1989;27:573–83.PubMedCrossRef
6.
go back to reference Wieslander G, Norbäck D, Lindgren T. Experimental exposure to propylene glycol mist in aviation emergency training: acute ocular and respiratory effects. Occup Environ Med. 2001;58:649–55.PubMedPubMedCentralCrossRef Wieslander G, Norbäck D, Lindgren T. Experimental exposure to propylene glycol mist in aviation emergency training: acute ocular and respiratory effects. Occup Environ Med. 2001;58:649–55.PubMedPubMedCentralCrossRef
8.
go back to reference Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. Vapors produced by electronic cigarettes and e-juices with flavorings induce toxicity, oxidative stress, and inflammatory response in lung epithelial cells and in mouse lung. PLoS One. 2015;10:e0116732.PubMedPubMedCentralCrossRef Lerner CA, Sundar IK, Yao H, Gerloff J, Ossip DJ, McIntosh S, Robinson R, Rahman I. Vapors produced by electronic cigarettes and e-juices with flavorings induce toxicity, oxidative stress, and inflammatory response in lung epithelial cells and in mouse lung. PLoS One. 2015;10:e0116732.PubMedPubMedCentralCrossRef
9.
go back to reference Schweitzer KS, Chen SX, Law S, Van Demark M, Poirier C, Justice MJ, Hubbard WC, Kim ES, Lai X, Wang M, et al. Endothelial disruptive proinflammatory effects of nicotine and e-cigarette vapor exposures. Am J Physiol Lung Cell Mol Physiol. 2015;309:L175–87.PubMedPubMedCentralCrossRef Schweitzer KS, Chen SX, Law S, Van Demark M, Poirier C, Justice MJ, Hubbard WC, Kim ES, Lai X, Wang M, et al. Endothelial disruptive proinflammatory effects of nicotine and e-cigarette vapor exposures. Am J Physiol Lung Cell Mol Physiol. 2015;309:L175–87.PubMedPubMedCentralCrossRef
10.
go back to reference Farsalinos KE, Romagna G, Allifranchini E, Ripamonti E, Bocchietto E, Todeschi S, Tsiapras D, Kyrzopoulos S, Voudris V. Comparison of the cytotoxic potential of cigarette smoke and electronic cigarette vapour extract on cultured myocardial cells. Int J Environ Res Public Health. 2013;10:5146–62.PubMedPubMedCentralCrossRef Farsalinos KE, Romagna G, Allifranchini E, Ripamonti E, Bocchietto E, Todeschi S, Tsiapras D, Kyrzopoulos S, Voudris V. Comparison of the cytotoxic potential of cigarette smoke and electronic cigarette vapour extract on cultured myocardial cells. Int J Environ Res Public Health. 2013;10:5146–62.PubMedPubMedCentralCrossRef
11.
go back to reference Romagna G, Allifranchini E, Bocchietto E, Todeschi S, Esposito M, Farsalinos KE. Cytotoxicity evaluation of electronic cigarette vapor extract on cultured mammalian fibroblasts (ClearStream-LIFE): comparison with tobacco cigarette smoke extract. Inhal Toxicol. 2013;25:354–61.PubMedCrossRef Romagna G, Allifranchini E, Bocchietto E, Todeschi S, Esposito M, Farsalinos KE. Cytotoxicity evaluation of electronic cigarette vapor extract on cultured mammalian fibroblasts (ClearStream-LIFE): comparison with tobacco cigarette smoke extract. Inhal Toxicol. 2013;25:354–61.PubMedCrossRef
12.
go back to reference Moses E, Wang T, Corbett S, Jackson GR, Drizik E, Perdomo C, Perdomo C, Kleerup E, Brooks D, O'Connor G, et al. Molecular impact of electronic cigarette aerosol exposure in human bronchial epithelium. Toxicol Sci. 2017;155:248–57.PubMedCrossRef Moses E, Wang T, Corbett S, Jackson GR, Drizik E, Perdomo C, Perdomo C, Kleerup E, Brooks D, O'Connor G, et al. Molecular impact of electronic cigarette aerosol exposure in human bronchial epithelium. Toxicol Sci. 2017;155:248–57.PubMedCrossRef
13.
go back to reference Misra M, Leverette RD, Cooper BT, Bennett MB, Brown SE. Comparative in vitro toxicity profile of electronic and tobacco cigarettes, smokeless tobacco and nicotine replacement therapy products: e-liquids, extracts and collected aerosols. Int J Environ Res Public Health. 2014;11:11325–47.PubMedPubMedCentralCrossRef Misra M, Leverette RD, Cooper BT, Bennett MB, Brown SE. Comparative in vitro toxicity profile of electronic and tobacco cigarettes, smokeless tobacco and nicotine replacement therapy products: e-liquids, extracts and collected aerosols. Int J Environ Res Public Health. 2014;11:11325–47.PubMedPubMedCentralCrossRef
14.
go back to reference Scheffler S, Dieken H, Krischenowski O, Forster C, Branscheid D, Aufderheide M. Evaluation of E-cigarette liquid vapor and mainstream cigarette smoke after direct exposure of primary human bronchial epithelial cells. Int J Environ Res Public Health. 2015;12:3915–25.PubMedPubMedCentralCrossRef Scheffler S, Dieken H, Krischenowski O, Forster C, Branscheid D, Aufderheide M. Evaluation of E-cigarette liquid vapor and mainstream cigarette smoke after direct exposure of primary human bronchial epithelial cells. Int J Environ Res Public Health. 2015;12:3915–25.PubMedPubMedCentralCrossRef
15.
go back to reference Cervellati F, Muresan XM, Sticozzi C, Gambari R, Montagner G, Forman HJ, Torricelli C, Maioli E, Valacchi G. Comparative effects between electronic and cigarette smoke in human keratinocytes and epithelial lung cells. Toxicol in Vitro. 2014;28:999–1005.PubMedPubMedCentralCrossRef Cervellati F, Muresan XM, Sticozzi C, Gambari R, Montagner G, Forman HJ, Torricelli C, Maioli E, Valacchi G. Comparative effects between electronic and cigarette smoke in human keratinocytes and epithelial lung cells. Toxicol in Vitro. 2014;28:999–1005.PubMedPubMedCentralCrossRef
16.
go back to reference Husari A, Shihadeh A, Talih S, Hashem Y, El Sabban M, Zaatari G. Acute exposure to electronic and combustible cigarette aerosols: effects in an animal model and in human alveolar cells. Nicotine Tob Res. 2016;18:613–9.PubMedCrossRef Husari A, Shihadeh A, Talih S, Hashem Y, El Sabban M, Zaatari G. Acute exposure to electronic and combustible cigarette aerosols: effects in an animal model and in human alveolar cells. Nicotine Tob Res. 2016;18:613–9.PubMedCrossRef
17.
go back to reference Yu V, Rahimy M, Korrapati A, Xuan Y, Zou AE, Krishnan AR, Tsui T, Aguilera JA, Advani S, Crotty Alexander LE, et al. Electronic cigarettes induce DNA strand breaks and cell death independently of nicotine in cell lines. Oral Oncol. 2016;52:58–65. Yu V, Rahimy M, Korrapati A, Xuan Y, Zou AE, Krishnan AR, Tsui T, Aguilera JA, Advani S, Crotty Alexander LE, et al. Electronic cigarettes induce DNA strand breaks and cell death independently of nicotine in cell lines. Oral Oncol. 2016;52:58–65.
18.
go back to reference Sussan TE, Gajghate S, Thimmulappa RK, Ma J, Kim J-H, Sudini K, Consolini N, Cormier SA, Lomnicki S, Hasan F, et al. Exposure to electronic cigarettes impairs pulmonary anti-bacterial and anti-viral defenses in a mouse model. PLoS One. 2015;10:e0116861.PubMedPubMedCentralCrossRef Sussan TE, Gajghate S, Thimmulappa RK, Ma J, Kim J-H, Sudini K, Consolini N, Cormier SA, Lomnicki S, Hasan F, et al. Exposure to electronic cigarettes impairs pulmonary anti-bacterial and anti-viral defenses in a mouse model. PLoS One. 2015;10:e0116861.PubMedPubMedCentralCrossRef
19.
go back to reference Behar RZ, Davis B, Wang Y, Bahl V, Lin S, Talbot P. Identification of toxicants in cinnamon-flavored electronic cigarette refill fluids. Toxicol in Vitro. 2013. Behar RZ, Davis B, Wang Y, Bahl V, Lin S, Talbot P. Identification of toxicants in cinnamon-flavored electronic cigarette refill fluids. Toxicol in Vitro. 2013.
20.
go back to reference Hutzler C, Paschke M, Kruschinski S, Henkler F, Hahn J, Luch A. Chemical hazards present in liquids and vapors of electronic cigarettes. Arch Toxicol. 2014;88:1295–308.PubMedCrossRef Hutzler C, Paschke M, Kruschinski S, Henkler F, Hahn J, Luch A. Chemical hazards present in liquids and vapors of electronic cigarettes. Arch Toxicol. 2014;88:1295–308.PubMedCrossRef
21.
go back to reference Sherwood CL, Boitano S. Airway epithelial cell exposure to distinct e-cigarette liquid flavorings reveals toxicity thresholds and activation of CFTR by the chocolate flavoring 2,5-dimethypyrazine. Respir Res. 2016;17:57.PubMedPubMedCentralCrossRef Sherwood CL, Boitano S. Airway epithelial cell exposure to distinct e-cigarette liquid flavorings reveals toxicity thresholds and activation of CFTR by the chocolate flavoring 2,5-dimethypyrazine. Respir Res. 2016;17:57.PubMedPubMedCentralCrossRef
22.
go back to reference Higham A, Rattray NJW, Dewhurst JA, Trivedi DK, Fowler SJ, Goodacre R, Singh D. Electronic cigarette exposure triggers neutrophil inflammatory responses. Respir Res. 2016;17:56.PubMedPubMedCentralCrossRef Higham A, Rattray NJW, Dewhurst JA, Trivedi DK, Fowler SJ, Goodacre R, Singh D. Electronic cigarette exposure triggers neutrophil inflammatory responses. Respir Res. 2016;17:56.PubMedPubMedCentralCrossRef
24.
go back to reference Shen Y, Wolkowicz MJ, Kotova T, Fan L, Timko MP. Transcriptome sequencing reveals e-cigarette vapor and mainstream-smoke from tobacco cigarettes activate different gene expression profiles in human bronchial epithelial cells. Sci Rep. 2016;6:23984.PubMedPubMedCentralCrossRef Shen Y, Wolkowicz MJ, Kotova T, Fan L, Timko MP. Transcriptome sequencing reveals e-cigarette vapor and mainstream-smoke from tobacco cigarettes activate different gene expression profiles in human bronchial epithelial cells. Sci Rep. 2016;6:23984.PubMedPubMedCentralCrossRef
25.
go back to reference Beisswenger C, Platz J, Seifart C, Vogelmeier C, Bals R. Exposure of differentiated airway epithelial cells to volatile smoke in vitro. Respiration. 2004;71:402–9.PubMedCrossRef Beisswenger C, Platz J, Seifart C, Vogelmeier C, Bals R. Exposure of differentiated airway epithelial cells to volatile smoke in vitro. Respiration. 2004;71:402–9.PubMedCrossRef
26.
go back to reference Bals R, Beisswenger C, Blouquit S, Chinet T. Isolation and air-liquid interface culture of human large airway and bronchiolar epithelial cells. J Cyst Fibros. 2004;3(Suppl 2):49–51.PubMedCrossRef Bals R, Beisswenger C, Blouquit S, Chinet T. Isolation and air-liquid interface culture of human large airway and bronchiolar epithelial cells. J Cyst Fibros. 2004;3(Suppl 2):49–51.PubMedCrossRef
27.
go back to reference Herr C, Beisswenger C, Hess C, Kandler K, Suttorp N, Welte T, Schroeder JM, Vogelmeier C, R Bals for the CAPNETZ Study Group. suppression of pulmonary innate host defence in smokers. Thorax. 2009;64:144–9.PubMedCrossRef Herr C, Beisswenger C, Hess C, Kandler K, Suttorp N, Welte T, Schroeder JM, Vogelmeier C, R Bals for the CAPNETZ Study Group. suppression of pulmonary innate host defence in smokers. Thorax. 2009;64:144–9.PubMedCrossRef
28.
go back to reference Fuoco FC, Buonanno G, Stabile L, Vigo P. Influential parameters on particle concentration and size distribution in the mainstream of e-cigarettes. Environ Pollut. 2014;184:523–9.PubMedCrossRef Fuoco FC, Buonanno G, Stabile L, Vigo P. Influential parameters on particle concentration and size distribution in the mainstream of e-cigarettes. Environ Pollut. 2014;184:523–9.PubMedCrossRef
29.
go back to reference Farsalinos KE, Spyrou A, Tsimopoulou K, Stefopoulos C, Romagna G, Voudris V. Nicotine absorption from electronic cigarette use: comparison between first and new-generation devices. Sci Rep. 2014;4:4133.PubMedPubMedCentralCrossRef Farsalinos KE, Spyrou A, Tsimopoulou K, Stefopoulos C, Romagna G, Voudris V. Nicotine absorption from electronic cigarette use: comparison between first and new-generation devices. Sci Rep. 2014;4:4133.PubMedPubMedCentralCrossRef
31.
go back to reference Dani JA, De Biasi M. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav. 2001;70:439–46.PubMedCrossRef Dani JA, De Biasi M. Cellular mechanisms of nicotine addiction. Pharmacol Biochem Behav. 2001;70:439–46.PubMedCrossRef
32.
go back to reference Chernyavsky AI, Shchepotin IB, Galitovkiy V, Grando SA. Mechanisms of tumor-promoting activities of nicotine in lung cancer: synergistic effects of cell membrane and mitochondrial nicotinic acetylcholine receptors. BMC Cancer. 2015;15:152.PubMedPubMedCentralCrossRef Chernyavsky AI, Shchepotin IB, Galitovkiy V, Grando SA. Mechanisms of tumor-promoting activities of nicotine in lung cancer: synergistic effects of cell membrane and mitochondrial nicotinic acetylcholine receptors. BMC Cancer. 2015;15:152.PubMedPubMedCentralCrossRef
33.
go back to reference Spindel ER, McEvoy CT. The role of nicotine in the effects of maternal smoking during pregnancy on lung development and childhood respiratory disease. Implications for Dangers of E-Cigarettes. Am J Respir Crit Care Med. 2016;193:486–94.PubMedPubMedCentralCrossRef Spindel ER, McEvoy CT. The role of nicotine in the effects of maternal smoking during pregnancy on lung development and childhood respiratory disease. Implications for Dangers of E-Cigarettes. Am J Respir Crit Care Med. 2016;193:486–94.PubMedPubMedCentralCrossRef
34.
go back to reference Jungnickel C, Wonnenberg B, Karabiber O, Wolf A, Voss M, Wolf L, Honecker A, Kamyschnikow A, Herr C, Bals R, Beisswenger C. Cigarette smoke-induced disruption of pulmonary barrier and bacterial translocation drive tumor-associated inflammation and growth. Am J Physiol Lung Cell Mol Physiol. 2015;309:L605–13.PubMedCrossRef Jungnickel C, Wonnenberg B, Karabiber O, Wolf A, Voss M, Wolf L, Honecker A, Kamyschnikow A, Herr C, Bals R, Beisswenger C. Cigarette smoke-induced disruption of pulmonary barrier and bacterial translocation drive tumor-associated inflammation and growth. Am J Physiol Lung Cell Mol Physiol. 2015;309:L605–13.PubMedCrossRef
35.
go back to reference Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25:402–8.CrossRefPubMed Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25:402–8.CrossRefPubMed
37.
go back to reference Komurov K, White MA, Ram PT. Use of data-biased random walks on graphs for the retrieval of context-specific networks from genomic data. PLoS Comput Biol. 2010;6. Komurov K, White MA, Ram PT. Use of data-biased random walks on graphs for the retrieval of context-specific networks from genomic data. PLoS Comput Biol. 2010;6.
39.
go back to reference Androutsopoulos VP, Tsatsakis AM, Spandidos DA. Cytochrome P450 CYP1A1: wider roles in cancer progression and prevention. BMC Cancer. 2009;9:1–17.CrossRef Androutsopoulos VP, Tsatsakis AM, Spandidos DA. Cytochrome P450 CYP1A1: wider roles in cancer progression and prevention. BMC Cancer. 2009;9:1–17.CrossRef
40.
go back to reference McNutt NS. The S100 family of multipurpose calcium-binding proteins. J Cutan Pathol. 1998;25:521–9.PubMedCrossRef McNutt NS. The S100 family of multipurpose calcium-binding proteins. J Cutan Pathol. 1998;25:521–9.PubMedCrossRef
41.
go back to reference Hiemstra PS, McCray PB Jr, Bals R. The innate immune function of airway epithelial cells in inflammatory lung disease. Eur Respir J. 2015;45:1150–62.PubMedPubMedCentralCrossRef Hiemstra PS, McCray PB Jr, Bals R. The innate immune function of airway epithelial cells in inflammatory lung disease. Eur Respir J. 2015;45:1150–62.PubMedPubMedCentralCrossRef
43.
go back to reference Voss M, Wonnenberg B, Honecker A, Kamyschnikow A, Herr C, Bischoff M, Tschernig T, Bals R, Beisswenger C. Cigarette smoke-promoted acquisition of bacterial pathogens in the upper respiratory tract leads to enhanced inflammation in mice. Respir Res. 2015;16:41.PubMedPubMedCentralCrossRef Voss M, Wonnenberg B, Honecker A, Kamyschnikow A, Herr C, Bischoff M, Tschernig T, Bals R, Beisswenger C. Cigarette smoke-promoted acquisition of bacterial pathogens in the upper respiratory tract leads to enhanced inflammation in mice. Respir Res. 2015;16:41.PubMedPubMedCentralCrossRef
44.
go back to reference Pace E, Ferraro M, Minervini M, Vitulo P, Pipitone L, Chiappara G, Siena L, Montalbano A, Johnson M, Gjomarkaj M. Beta Defensin-2 is reduced in central but not in distal Airways of Smoker COPD patients. PLoS One. 2012;7:e33601.PubMedPubMedCentralCrossRef Pace E, Ferraro M, Minervini M, Vitulo P, Pipitone L, Chiappara G, Siena L, Montalbano A, Johnson M, Gjomarkaj M. Beta Defensin-2 is reduced in central but not in distal Airways of Smoker COPD patients. PLoS One. 2012;7:e33601.PubMedPubMedCentralCrossRef
45.
go back to reference Hwang JH, Lyes M, Sladewski K, Enany S, McEachern E, Mathew DP, Das S, Moshensky A, Bapat S, Pride DT, et al. Electronic cigarette inhalation alters innate immunity and airway cytokines while increasing the virulence of colonizing bacteria. J Mol Med (Berl). 2016;94(6):667–79. Hwang JH, Lyes M, Sladewski K, Enany S, McEachern E, Mathew DP, Das S, Moshensky A, Bapat S, Pride DT, et al. Electronic cigarette inhalation alters innate immunity and airway cytokines while increasing the virulence of colonizing bacteria. J Mol Med (Berl). 2016;94(6):667–79.
46.
go back to reference Martin EM, Clapp PW, Rebuli ME, Pawlak EA, Glista-Baker E, Benowitz NL, Fry RC, Jaspers I. E-cigarette use results in suppression of immune and inflammatory-response genes in nasal epithelial cells similar to cigarette smoke. American journal of physiology Lung cellular and molecular physiology. 2016;311:L135–44.PubMedPubMedCentralCrossRef Martin EM, Clapp PW, Rebuli ME, Pawlak EA, Glista-Baker E, Benowitz NL, Fry RC, Jaspers I. E-cigarette use results in suppression of immune and inflammatory-response genes in nasal epithelial cells similar to cigarette smoke. American journal of physiology Lung cellular and molecular physiology. 2016;311:L135–44.PubMedPubMedCentralCrossRef
47.
go back to reference Wu Q, Jiang D, Minor M, Chu HW. Electronic cigarette liquid increases inflammation and virus infection in primary human airway epithelial cells. PLoS One. 2014;9:e108342.PubMedPubMedCentralCrossRef Wu Q, Jiang D, Minor M, Chu HW. Electronic cigarette liquid increases inflammation and virus infection in primary human airway epithelial cells. PLoS One. 2014;9:e108342.PubMedPubMedCentralCrossRef
48.
go back to reference Alexander LEC, Shin S, Hwang JH. Infl ammatory diseases of the lung induced by conventional cigarette smoke a review. Chest. 2015;148:1307–22.CrossRef Alexander LEC, Shin S, Hwang JH. Infl ammatory diseases of the lung induced by conventional cigarette smoke a review. Chest. 2015;148:1307–22.CrossRef
49.
go back to reference Rastrick JM, Stevenson CS, Eltom S, Grace M, Davies M, Kilty I, Evans SM, Pasparakis M, Catley MC, Lawrence T, et al. Cigarette smoke induced airway inflammation is independent of NF-kappaB signalling. PLoS One. 2013;8:e54128.PubMedPubMedCentralCrossRef Rastrick JM, Stevenson CS, Eltom S, Grace M, Davies M, Kilty I, Evans SM, Pasparakis M, Catley MC, Lawrence T, et al. Cigarette smoke induced airway inflammation is independent of NF-kappaB signalling. PLoS One. 2013;8:e54128.PubMedPubMedCentralCrossRef
50.
go back to reference Heijink IH, de Bruin HG, van den Berge M, Bennink LJC, Brandenburg SM, Gosens R, van Oosterhout AJ, Postma DS. Role of aberrant WNT signalling in the airway epithelial response to cigarette smoke in chronic obstructive pulmonary disease. Thorax. 2013;68:709–16.PubMedCrossRef Heijink IH, de Bruin HG, van den Berge M, Bennink LJC, Brandenburg SM, Gosens R, van Oosterhout AJ, Postma DS. Role of aberrant WNT signalling in the airway epithelial response to cigarette smoke in chronic obstructive pulmonary disease. Thorax. 2013;68:709–16.PubMedCrossRef
51.
go back to reference Gerloff J, Sundar IK, Freter R, Sekera ER, Friedman AE, Robinson R, Pagano T, Rahman I. Inflammatory response and barrier dysfunction by different e-cigarette flavoring chemicals identified by gas chromatography-mass spectrometry in e-liquids and e-vapors on human lung epithelial cells and fibroblasts. Appl In Vitro Toxicol. 2017;3:28–40.PubMedPubMedCentralCrossRef Gerloff J, Sundar IK, Freter R, Sekera ER, Friedman AE, Robinson R, Pagano T, Rahman I. Inflammatory response and barrier dysfunction by different e-cigarette flavoring chemicals identified by gas chromatography-mass spectrometry in e-liquids and e-vapors on human lung epithelial cells and fibroblasts. Appl In Vitro Toxicol. 2017;3:28–40.PubMedPubMedCentralCrossRef
52.
go back to reference Husari A, Shihadeh A, Talih S, Hashem Y, El Sabban M, Zaatari G. Acute exposure to electronic and combustible cigarette aerosols: effects in an animal model and in human alveolar cells. Nicotine Tob Res. 2015. Husari A, Shihadeh A, Talih S, Hashem Y, El Sabban M, Zaatari G. Acute exposure to electronic and combustible cigarette aerosols: effects in an animal model and in human alveolar cells. Nicotine Tob Res. 2015.
53.
go back to reference Nakamura H, Masutani H, Yodoi J. Extracellular thioredoxin and thioredoxin-binding protein 2 in control of cancer. Semin Cancer Biol. 2006;16:444–51.PubMedCrossRef Nakamura H, Masutani H, Yodoi J. Extracellular thioredoxin and thioredoxin-binding protein 2 in control of cancer. Semin Cancer Biol. 2006;16:444–51.PubMedCrossRef
54.
go back to reference Marenholz I, Lovering RC, Heizmann CW. An update of the S100 nomenclature. Biochim Biophys Acta. 1763;2006:1282–3. Marenholz I, Lovering RC, Heizmann CW. An update of the S100 nomenclature. Biochim Biophys Acta. 1763;2006:1282–3.
56.
go back to reference Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999;97:889–901.PubMedCrossRef Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999;97:889–901.PubMedCrossRef
57.
go back to reference Kang JH, Hwang SM, Chung IY. S100A8, S100A9 and S100A12 activate airway epithelial cells to produce MUC5AC via extracellular signal-regulated kinase and nuclear factor-κB pathways. Immunology. 2015;144:79–90.PubMedCrossRef Kang JH, Hwang SM, Chung IY. S100A8, S100A9 and S100A12 activate airway epithelial cells to produce MUC5AC via extracellular signal-regulated kinase and nuclear factor-κB pathways. Immunology. 2015;144:79–90.PubMedCrossRef
58.
go back to reference Solleti SK, Bhattacharya S, Ahmad A, Wang Q, Mereness J, Rangasamy T, Mariani TJ. MicroRNA expression profiling defines the impact of electronic cigarettes on human airway epithelial cells. Sci Rep. 2017;7:1081.PubMedPubMedCentralCrossRef Solleti SK, Bhattacharya S, Ahmad A, Wang Q, Mereness J, Rangasamy T, Mariani TJ. MicroRNA expression profiling defines the impact of electronic cigarettes on human airway epithelial cells. Sci Rep. 2017;7:1081.PubMedPubMedCentralCrossRef
59.
go back to reference Aug A, Altraja S, Kilk K, Porosk R, Soomets U, Altraja A. E-cigarette affects the Metabolome of primary Normal human bronchial epithelial cells. PLoS One. 2015;10:e0142053.PubMedPubMedCentralCrossRef Aug A, Altraja S, Kilk K, Porosk R, Soomets U, Altraja A. E-cigarette affects the Metabolome of primary Normal human bronchial epithelial cells. PLoS One. 2015;10:e0142053.PubMedPubMedCentralCrossRef
60.
go back to reference Ganapathy V, Manyanga J, Brame L, McGuire D, Sadhasivam B, Floyd E, Rubenstein DA, Ramachandran I, Wagener T, Queimado L. Electronic cigarette aerosols suppress cellular antioxidant defenses and induce significant oxidative DNA damage. PLoS One. 2017;12:e0177780.PubMedPubMedCentralCrossRef Ganapathy V, Manyanga J, Brame L, McGuire D, Sadhasivam B, Floyd E, Rubenstein DA, Ramachandran I, Wagener T, Queimado L. Electronic cigarette aerosols suppress cellular antioxidant defenses and induce significant oxidative DNA damage. PLoS One. 2017;12:e0177780.PubMedPubMedCentralCrossRef
61.
go back to reference Scheffler S, Dieken H, Krischenowski O, Aufderheide M. Cytotoxic evaluation of e-liquid aerosol using different lung-derived cell models. Int J Environ Res Public Health. 2015;12:12466–74.PubMedPubMedCentralCrossRef Scheffler S, Dieken H, Krischenowski O, Aufderheide M. Cytotoxic evaluation of e-liquid aerosol using different lung-derived cell models. Int J Environ Res Public Health. 2015;12:12466–74.PubMedPubMedCentralCrossRef
62.
go back to reference Rowell TR, Reeber SL, Lee SL, Harris RA, Nethery RC, Herring AH, Glish GL, Tarran R. Flavored e-cigarette liquids reduce proliferation and viability in the CALU3 airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol. 2017;313:L52–l66.PubMedPubMedCentralCrossRef Rowell TR, Reeber SL, Lee SL, Harris RA, Nethery RC, Herring AH, Glish GL, Tarran R. Flavored e-cigarette liquids reduce proliferation and viability in the CALU3 airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol. 2017;313:L52–l66.PubMedPubMedCentralCrossRef
63.
go back to reference Taylor M, Carr T, Oke O, Jaunky T, Breheny D, Lowe F, Gaca M. E-cigarette aerosols induce lower oxidative stress in vitro when compared to tobacco smoke. Toxicol Mech Methods. 2016;26:465–76.PubMedCrossRef Taylor M, Carr T, Oke O, Jaunky T, Breheny D, Lowe F, Gaca M. E-cigarette aerosols induce lower oxidative stress in vitro when compared to tobacco smoke. Toxicol Mech Methods. 2016;26:465–76.PubMedCrossRef
64.
go back to reference Fogh J, Fogh JM, Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst. 1977;59:221–6.PubMedCrossRef Fogh J, Fogh JM, Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst. 1977;59:221–6.PubMedCrossRef
65.
go back to reference Kosmider L, Sobczak A, Fik M, Knysak J, Zaciera M, Kurek J, Goniewicz ML. Carbonyl compounds in electronic cigarette vapors: effects of nicotine solvent and battery output voltage. Nicotine Tob Res. 2014;16:1319–26.PubMedPubMedCentralCrossRef Kosmider L, Sobczak A, Fik M, Knysak J, Zaciera M, Kurek J, Goniewicz ML. Carbonyl compounds in electronic cigarette vapors: effects of nicotine solvent and battery output voltage. Nicotine Tob Res. 2014;16:1319–26.PubMedPubMedCentralCrossRef
66.
go back to reference Benowitz NL, Jacob P 3rd, Bernert JT, Wilson M, Wang L, Allen F, Dempsey D. Carcinogen exposure during short-term switching from regular to "light" cigarettes. Cancer Epidemiol Biomark Prev. 2005;14:1376–83.CrossRef Benowitz NL, Jacob P 3rd, Bernert JT, Wilson M, Wang L, Allen F, Dempsey D. Carcinogen exposure during short-term switching from regular to "light" cigarettes. Cancer Epidemiol Biomark Prev. 2005;14:1376–83.CrossRef
67.
go back to reference Haswell LE, Baxter A, Banerjee A, Verrastro I, Mushonganono J, Adamson J, Thorne D, Gaca M, Minet E. Reduced biological effect of e-cigarette aerosol compared to cigarette smoke evaluated in vitro using normalized nicotine dose and RNA-seq-based toxicogenomics. Sci Rep. 2017;7:888.PubMedPubMedCentralCrossRef Haswell LE, Baxter A, Banerjee A, Verrastro I, Mushonganono J, Adamson J, Thorne D, Gaca M, Minet E. Reduced biological effect of e-cigarette aerosol compared to cigarette smoke evaluated in vitro using normalized nicotine dose and RNA-seq-based toxicogenomics. Sci Rep. 2017;7:888.PubMedPubMedCentralCrossRef
68.
go back to reference Antherieu S, Garat A, Beauval N, Soyez M, Allorge D, Garcon G, Lo-Guidice JM. Comparison of cellular and transcriptomic effects between electronic cigarette vapor and cigarette smoke in human bronchial epithelial cells. Toxicol in Vitro. 2017;45:417–25.PubMedCrossRef Antherieu S, Garat A, Beauval N, Soyez M, Allorge D, Garcon G, Lo-Guidice JM. Comparison of cellular and transcriptomic effects between electronic cigarette vapor and cigarette smoke in human bronchial epithelial cells. Toxicol in Vitro. 2017;45:417–25.PubMedCrossRef
Metadata
Title
Cigarette smoke and electronic cigarettes differentially activate bronchial epithelial cells
Authors
Christian Herr
Konstantinos Tsitouras
Julia Niederstraßer
Christina Backes
Christoph Beisswenger
Li Dong
Loïc Guillot
Andreas Keller
Robert Bals
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Respiratory Research / Issue 1/2020
Electronic ISSN: 1465-993X
DOI
https://doi.org/10.1186/s12931-020-1317-2

Other articles of this Issue 1/2020

Respiratory Research 1/2020 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.