Evaluation of Calu-3 cell lines as an in vitro model to study the inhalation toxicity of flavoring extracts

References

• Alfaro-Moreno E, Torres V, Miranda J, Martínez L, García-Cuellar C, Nawrot TS, Vanaudenaerde B, Hoet P, Ramírez-López P, Rosas I, et al. 2009. Induction of IL-6 and inhibition of IL-8 secretion in the human airway cell line Calu-3 by urban particulate matter collected with a modified method of PM sampling. Environ Res. 109(5):528–535.
   PubMed Web of Science ®Google Scholar
• Amatngalim GD, Broekman W, Daniel NM, van der Vlugt LE, van Schadewijk A, Taube C, Hiemstra PS. 2016. Cigarette smoke modulates repair and innate immunity following injury to airway epithelial cells. PLoS One. 11(11):e0166255.
   PubMed Web of Science ®Google Scholar
• Anderson JM, Van Itallie CM. 1995. Tight junctions and the molecular basis for regulation of paracellular permeability. Am J Physiol. 269(4 Pt 1):G467–G475.
   PubMed Web of Science ®Google Scholar
• Andreoli C, Gigante D, Nunziata A. 2003. A review of in vitro methods to assess the biological activity of tobacco smoke with the aim of reducing the toxicity of smoke. Toxicol In Vitro. 17(5–6):587–594.
   PubMed Web of Science ®Google Scholar
• Bakand S, Hayes A. 2010. Troubleshooting methods for toxicity testing of airborne chemicals in vitro. J Pharmacol Toxicol Methods. 61(2):76–85.
   PubMed Web of Science ®Google Scholar
• Balharry D, Sexton K, BeruBe KA. 2008. An in vitro approach to assess the toxicity of inhaled tobacco smoke components: nicotine, cadmium, formaldehyde and urethane. Toxicology. 244(1):66–76.
   PubMed Web of Science ®Google Scholar
• Balogh Sivars K, Sivars U, Hornberg E, Zhang H, Brändén L, Bonfante R, Huang S, Constant S, Robinson I, Betts CJ, et al. 2018. A 3D human airway model enables prediction of respiratory toxicity of inhaled drugs in vitro. Toxicol Sci. 162(1):301–308.
   PubMed Web of Science ®Google Scholar
• Cavet ME, West M, Simmons NL. 1997. Transepithelial transport of the fluoroquinolone ciprofloxacin by human airway epithelial Calu-3 cells. Antimicrob Agents Chemother. 41(12):2693–2698.
   PubMed Web of Science ®Google Scholar
• Chen S, Einspanier R, Schoen J. 2015. Transepithelial electrical resistance (TEER): a functional parameter to monitor the quality of oviduct epithelial cells cultured on filter supports. Histochem Cell Biol. 144(5):509–515.
   PubMed Web of Science ®Google Scholar
• Clapp PW, Jaspers I. 2017. Electronic cigarettes: their constituents and potential links to asthma. Curr Allergy Asthma Rep. 17(11):79.
   PubMed Web of Science ®Google Scholar
• Devor DC, Singh AK, Lambert LC, DeLuca A, Frizzell RA, Bridges RJ. 1999. Bicarbonate and chloride secretion in Calu-3 human airway epithelial cells. J Gen Physiol. 113(5):743–760.
   PubMed Web of Science ®Google Scholar
• Ehrhardt C, Fiegel J, Fuchs S, Abu-Dahab R, Schaefer UF, Hanes J, Lehr CM. 2002. Drug absorption by the respiratory mucosa: cell culture models and particulate drug carriers. J Aerosol Med. 15(2):131–139.
   PubMedGoogle Scholar
• Fetterman JL, Weisbrod RM, Feng B, Bastin R, Tuttle ST, Holbrook M, Baker G, Robertson RM, Conklin DJ, Bhatnagar A, et al. 2018. Flavorings in tobacco products induce endothelial cell dysfunction arterioscler. Arterioscler Thromb Vasc Biol. 38(7):1607–1615.
   PubMed Web of Science ®Google Scholar
• Fink MP, Delude RL. 2005. Epithelial barrier dysfunction: a unifying theme to explain the pathogenesis of multiple organ dysfunction at the cellular level. Crit Care Clin. 21(2):177–196.
   PubMed Web of Science ®Google Scholar
• Foster KA, Avery ML, Yazdanian M, Audus KL. 2000. Characterization of the Calu-3 cell line as a tool to screen pulmonary drug delivery. Int J Pharm. 208(1–2):1–11.
   PubMedGoogle Scholar
• Gonzalez-Suarez I, Martin F, Marescotti D, Guedj E, Acali S, Johne S, Dulize R, Baumer K, Peric D, Goedertier D, et al. 2016. In vitro systems toxicology assessment of a candidate modified risk tobacco product shows reduced toxicity compared to that of a conventional cigarette. Chem Res Toxicol. 29(1):3–18.
   PubMed Web of Science ®Google Scholar
• Harcourt JL, Caidi H, Anderson LJ, Haynes LM. 2011. Evaluation of the Calu-3 cell line as a model of in vitro respiratory syncytial virus infection. J Virol Methods. 174(1–2):144–149.
   PubMed Web of Science ®Google Scholar
• Harcourt JL, Haynes LM. 2013. Establishing a liquid-covered culture of polarized human airway epithelial Calu-3 cells to study host cell response to respiratory pathogens in vitro. J Vis Exp. (72):e50157. doi:https://doi.org/10.3791/50157
   Google Scholar
• Hiemstra PS, Grootaers G, van der Does AM, Krul CAM, Kooter IM. 2018. Human lung epithelial cell cultures for analysis of inhaled toxicants: lessons learned and future directions. Toxicol In Vitro. 47:137–146.
   PubMed Web of Science ®Google Scholar
• Ihekwereme C, Esimone C, Shao D, Agu RU. 2014. Preliminary studies on validation of calu-3 cell line as a model for screening respiratory mucosa irritation and toxicity. Pharmaceutics. 6(2):268–280.
   PubMedGoogle Scholar
• Institute of Medicine (U.S.). Committee on Scientific Standards for Studies on Modified Risk Tobacco Products. 2012. Scientific standards for studies on modified risk tobacco products. Washington, DC: National Academies Press.
   Google Scholar
• Jeong MH, Kim HR, Bang IJ, Yoo SH, Lee SJ, Lee KH, Chung KH. 2019. In vitro model for predicting acute inhalation toxicity by using a Calu-3 epithelium cytotoxicity assay. J Pharmacol Toxicol Methods. 98:106576.
   PubMed Web of Science ®Google Scholar
• Jia M, Zhang Y, Zhang H, Qin Q, Xu CB. 2019. Cigarette smoke particles-induced airway hyperreactivity in vivo and in vitro. Biol Pharm Bull. 42(5):703–711.
   PubMed Web of Science ®Google Scholar
• Kreft ME, Jerman UD, Lasic E, Hevir-Kene N, Rizner TL, Peternel L, Kristan K. 2015. The characterization of the human cell line Calu-3 under different culture conditions and its use as an optimized in vitro model to investigate bronchial epithelial function. Eur J Pharm Sci. 69:1–9.
   PubMed Web of Science ®Google Scholar
• Leigh NJ, Tran PL, O'Connor RJ, Goniewicz ML. 2018. Cytotoxic effects of heated tobacco products (HTP) on human bronchial epithelial cells. Tob Control. 27(Suppl 1):s26–s29.
   PubMedGoogle Scholar
• Li X. 2016. In vitro toxicity testing of cigarette smoke based on the air-liquid interface exposure: a review. Toxicol In Vitro. 36:105–113.
   PubMed Web of Science ®Google Scholar
• Lillehoj EP, Kato K, Lu W, Kim KC. 2013. Cellular and molecular biology of airway mucins. Int Rev Cell Mol Biol. 303:139–202.
   PubMed Web of Science ®Google Scholar
• Mathia NR, Timoszyk J, Stetsko PI, Megill JR, Smith RL, Wall DA. 2002. Permeability characteristics of Calu-3 human bronchial epithelial cells: in vitro-in vivo correlation to predict lung absorption in rats. J Drug Target. 10(1):31–40.
   PubMed Web of Science ®Google Scholar
• Maunders H, Patwardhan S, Phillips J, Clack A, Richter A. 2007. Human bronchial epithelial cell transcriptome: gene expression changes following acute exposure to whole cigarette smoke in vitro. Am J Physiol Lung Cell Mol Physiol. 292(5):L1248–L1256.
   PubMed Web of Science ®Google Scholar
• Mukherjee M, Pritchard DI, Bosquillon C. 2012. Evaluation of air-interfaced Calu-3 cell layers for investigation of inhaled drug interactions with organic cation transporters in vitro. Int J Pharm. 426(1–2):7–14.
   PubMed Web of Science ®Google Scholar
• Nara H, Fukano Y, Nishino T, Aufderheide M. 2013. Detection of the cytotoxicity of water-insoluble fraction of cigarette smoke by direct exposure to cultured cells at an air-liquid interface. Exp Toxicol Pathol. 65(5):683–688.
   PubMedGoogle Scholar
• Neilson L, Mankus C, Thorne D, Jackson G, DeBay J, Meredith C. 2015. Development of an in vitro cytotoxicity model for aerosol exposure using 3D reconstructed human airway tissue; application for assessment of e-cigarette aerosol. Toxicol In Vitro. 29(7):1952–1962.
   PubMed Web of Science ®Google Scholar
• Ong HX, Traini D, Young PM. 2013. Pharmaceutical applications of the Calu-3 lung epithelia cell line. Expert Opin Drug Deliv. 10(9):1287–1302.
   PubMed Web of Science ®Google Scholar
• Paumgartten FJR, Gomes-Carneiro MR, Oliveira A. 2017. The impact of tobacco additives on cigarette smoke toxicity: a critical appraisal of tobacco industry studies. Cad Saude Publica. 33 (Suppl 3):e00132415.
   Google Scholar
• Phillips J, Kluss B, Richter A, Massey E. 2005. Exposure of bronchial epithelial cells to whole cigarette smoke: assessment of cellular responses. Altern Lab Anim. 33(3):239–248.
   PubMed Web of Science ®Google Scholar
• Rothen-Rutishauser B, Blank F, Muhlfeld C, Gehr P. 2008. In vitro models of the human epithelial airway barrier to study the toxic potential of particulate matter. Expert Opin Drug Metab Toxicol. 4(8):1075–1089.
   PubMed Web of Science ®Google Scholar
• Seibel J, Kryshen K, Pongracz JE, Lehner MD. 2018. In vivo and in vitro investigation of anti-inflammatory and mucus-regulatory activities of a fixed combination of thyme and primula extracts. Pulm Pharmacol Ther. 51:10–17.
   PubMed Web of Science ®Google Scholar
• Simet SM, Sisson JH, Pavlik JA, Devasure JM, Boyer C, Liu X, Kawasaki S, Sharp JG, Rennard SI, Wyatt TA, et al. 2010. Long-term cigarette smoke exposure in a mouse model of ciliated epithelial cell function. Am J Respir Cell Mol Biol. 43(6):635–640.
   PubMed Web of Science ®Google Scholar
• Sørli JB, Huang Y, Da Silva E, Hansen JS, Zuo YY, Frederiksen M, Nørgaard AW, Ebbehøj NE, Larsen ST, Hougaard KS, et al. 2018. Prediction of acute inhalation toxicity using in vitro lung surfactant inhibition. Altex. 35(1):26–36.
   PubMedGoogle Scholar
• Sorli JB, Hansen JS, Norgaard AW, Levin M, Larsen ST. 2015. An in vitro method for predicting inhalation toxicity of impregnation spray products. Altex. 32(2):101–111.
   PubMedGoogle Scholar
• Wan H, Winton HL, Soeller C, Stewart GA, Thompson PJ, Gruenert DC, Cannell MB, Garrod DR, Robinson C. 2000. Tight junction properties of the immortalized human bronchial epithelial cell lines Calu-3 and 16HBE14o. Eur Respir J. 15(6):1058–1068.
   PubMed Web of Science ®Google Scholar