In vitro genotoxicity of dibutyl phthalate on A549 lung cells at air-liquid interface in exposure concentrations relevant at workplaces.


Journal

Environmental and molecular mutagenesis
ISSN: 1098-2280
Titre abrégé: Environ Mol Mutagen
Pays: United States
ID NLM: 8800109

Informations de publication

Date de publication:
11 2021
Historique:
revised: 14 09 2021
received: 19 07 2021
accepted: 07 10 2021
pubmed: 13 10 2021
medline: 18 12 2021
entrez: 12 10 2021
Statut: ppublish

Résumé

The ubiquitous use of phthalates in various materials and the knowledge about their potential adverse effects is of great concern for human health. Several studies have uncovered their role in carcinogenic events and suggest various phthalate-associated adverse health effects that include pulmonary diseases. However, only limited information on pulmonary toxicity is available considering inhalation of phthalates as the route of exposure. While in vitro studies are often based on submerged exposures, this study aimed to expose A549 alveolar epithelial cells at the air-liquid interface (ALI) to unravel the genotoxic and oxidative stress-inducing potential of dibutyl phthalate (DBP) with concentrations relevant at occupational settings. Within this scope, a computer modeling approach calculating alveolar deposition of DBP particles in the human lung was used to define in vitro ALI exposure conditions comparable to potential occupational DBP exposures. The deposited mass of DBP ranged from 0.03 to 20 ng/cm

Identifiants

pubmed: 34636079
doi: 10.1002/em.22464
doi:

Substances chimiques

Air Pollutants, Occupational 0
Mutagens 0
Plasticizers 0
Dibutyl Phthalate 2286E5R2KE
Malondialdehyde 4Y8F71G49Q

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

490-501

Informations de copyright

© 2021 The Authors. Environmental and Molecular Mutagenesis published by Wiley Periodicals LLC on behalf of Environmental Mutagen Society.

Références

Al-Saleh, I., Al-Rajudi, T., Al-Qudaihi, G. & Manogaran, P. (2017) Evaluating the potential genotoxicity of phthalates esters (PAEs) in perfumes using in vitro assays. Environmental Science and Pollution Research International, 24(30), 23903-23914. https://doi.org/10.1007/s11356-017-9978-1
Andersen, C., Krais, A.M., Eriksson, A.C., Jakobsson, J., Löndahl, J., Nielsen, J. et al. (2018) Inhalation and dermal uptake of particle and gas-phase phthalates-a human exposure study. Environmental Science & Technology, 52(21), 12792-12800. https://doi.org/10.1021/acs.est.8b03761
Ayala, A., Munoz, M.F. & Arguelles, S. (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 2014, 360438-360431. https://doi.org/10.1155/2014/360438
Benli, A.C., Erkmen, B. & Erkoc, F. (2016) Genotoxicity of sub-lethal di-n-butyl phthalate (DBP) in Nile tilapia (Oreochromis niloticus). Arhiv za Higijenu Rada i Toksikologiju, 67(1), 25-30. https://doi.org/10.1515/aiht-2016-67-2723
Boniol, M., Koechlin, A. & Boyle, P. (2017) Meta-analysis of occupational exposures in the rubber manufacturing industry and risk of cancer. International Journal of Epidemiology, 46(6), 1940-1947. https://doi.org/10.1093/ije/dyx146
Campanale, C., Massarelli, C., Savino, I., Locaputo, V. & Uricchio, V.F. (2020) A detailed review study on potential effects of microplastics and additives of concern on human health. International Journal of Environmental Research and Public Health, 17(4), 1212. https://doi.org/10.3390/ijerph17041212
Chatterjee, N. & Walker, G.C. (2017) Mechanisms of DNA damage, repair, and mutagenesis. Environmental and Molecular Mutagenesis, 58(5), 235-263. https://doi.org/10.1002/em.22087
Cheresh, P., Kim, S.J., Tulasiram, S. & Kamp, D.W. (2013) Oxidative stress and pulmonary fibrosis. Biochimica et Biophysica Acta, 1832(7), 1028-1040. https://doi.org/10.1016/j.bbadis.2012.11.021
Chi, C., Xia, M., Zhou, C., Wang, X., Weng, M. & Shen, X. (2017) Determination of 15 phthalate esters in air by gas-phase and particle-phase simultaneous sampling. Journal of Environmental Sciences (China), 55, 137-145. https://doi.org/10.1016/j.jes.2016.01.036
Ching, J. & Kajino, M. (2018) Aerosol mixing state matters for particles deposition in human respiratory system. Scientific Reports, 8(1), 8864. https://doi.org/10.1038/s41598-018-27156-z
Committee, E.S., More, S.J., Bampidis, V., Bragard, C., Halldorsson, T.I., Hernandez-Jerez, A.F. et al. (2021) Guidance on aneugenicity assessment. EFSA Journal, 19(8), e06770. https://doi.org/10.2903/j.efsa.2021.6770
Di Bucchianico, S., Cappellini, F., Le Bihanic, F., Zhang, Y., Dreij, K. & Karlsson, H.L. (2017) Genotoxicity of TiO2 nanoparticles assessed by mini-gel comet assay and micronucleus scoring with flow cytometry. Mutagenesis, 32(1), 127-137. https://doi.org/10.1093/mutage/gew030
Di Bucchianico, S., Migliore, L., Marsili, P., Vergari, C., Giammanco, F. & Giorgetti, E. (2015) Cyto- and genotoxicity assessment of Gold nanoparticles obtained by laser ablation in A549 lung adenocarcinoma cells. Journal of Nanoparticle Research, 17(5), 213. https://doi.org/10.1007/s11051-015-3023-4
Ding, Y., Weindl, P., Lenz, A.G., Mayer, P., Krebs, T. & Schmid, O. (2020) Quartz crystal microbalances (QCM) are suitable for real-time dosimetry in nanotoxicological studies using VITROCELL(R)Cloud cell exposure systems. Particle and Fibre Toxicology, 17(1), 44. https://doi.org/10.1186/s12989-020-00376-w
Du, L., Li, G., Liu, M., Li, Y., Yin, S., Zhao, J. et al. (2015) Evaluation of DNA damage and antioxidant system induced by di-n-butyl phthalates exposure in earthworms (Eisenia fetida). Ecotoxicology and Environmental Safety, 115, 75-82. https://doi.org/10.1016/j.ecoenv.2015.01.031
ECB. (2003) European Union risk assessment report on Dibutyl phthalate-addendum to the environmental section 2004. In: SJM, B.G.H., Allanou, R., Berthault, F., de Bruijn, J., Luotamo, M., Musset, C. et al. (Eds.) European chemicals agency (ECHA), Vol. 29. Luxembourg: Office for Official Publications of the European Communities.
Elhajouji, A., Lukamowicz, M., Cammerer, Z. & Kirsch-Volders, M. (2011) Potential thresholds for genotoxic effects by micronucleus scoring. Mutagenesis, 26(1), 199-204. https://doi.org/10.1093/mutage/geq089
Elhajouji, A., Van Hummelen, P. & Kirsch-Volders, M. (1995) Indications for a threshold of chemically-induced aneuploidy in vitro in human lymphocytes. Environmental and Molecular Mutagenesis, 26(4), 292-304. https://doi.org/10.1002/em.2850260405
Erkekoglu, P. & Kocer-Gumusel, B. (2014) Genotoxicity of phthalates. Toxicology Mechanisms and Methods, 24(9), 616-626. https://doi.org/10.3109/15376516.2014.960987
Ferron, G.A., Upadhyay, S., Zimmermann, R. & Karg, E. (2013) Model of the deposition of aerosol particles in the respiratory tract of the rat. II. Hygroscopic particle deposition. J Aerosol Med Pulm Drug Deliv, 26(2), 101-119. https://doi.org/10.1089/jamp.2011.0965
Frery, N., Santonen, T., Porras, S.P., Fucic, A., Leso, V., Bousoumah, R. et al. (2020) Biomonitoring of occupational exposure to phthalates: a systematic review. International Journal of Hygiene and Environmental Health, 229, 113548. https://doi.org/10.1016/j.ijheh.2020.113548
Garcia-Canton, C., Minet, E., Anadon, A. & Meredith, C. (2013) Metabolic characterization of cell systems used in in vitro toxicology testing: lung cell system BEAS-2B as a working example. Toxicology In Vitro, 27(6), 1719-1727. https://doi.org/10.1016/j.tiv.2013.05.001
Hartwig, A., Papameletiou, D., & Klein, C.L. (2017) Recommendation from the Scientific Committee on Occupational Exposure Limits-SCOEL/REC/143 Di-n-butyl phthalate. Directorate-General for Employment, Social Affairs and Inclusion (European Commission), SCOEL, Luxembourg: Publications Office of the European Union. doi: https://doi.org/10.2767/972673
Hines, C.J., Hopf, N.B., Deddens, J.A., Silva, M.J. & Calafat, A.M. (2011) Estimated daily intake of phthalates in occupationally exposed groups. Journal of Exposure Science & Environmental Epidemiology, 21(2), 133-141. https://doi.org/10.1038/jes.2009.62
Hou, J., Yin, W., Li, P., Hu, C., Xu, T., Cheng, J. et al. (2020) Joint effect of polycyclic aromatic hydrocarbons and phthalates exposure on telomere length and lung function. Journal of Hazardous Materials, 386, 121663. https://doi.org/10.1016/j.jhazmat.2019.121663
Hsieh, T.H., Tsai, C.F., Hsu, C.Y., Kuo, P.L., Lee, J.N., Chai, C.Y. et al. (2012) Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway. The FASEB Journal, 26(2), 778-787. https://doi.org/10.1096/fj.11-191742
Karg, E.W., Ferron, G.A., Bauer, S., Di Bucchianico, S. & Zimmermann, R. (2020) Is the particle deposition in a cell exposure facility comparable to the lungs? A computer model approach. Aerosol Science and Technology, 54(6), 668-684. https://doi.org/10.1080/02786826.2020.1724868
Kashyap, D. & Agarwal, T. (2018) Concentration and factors affecting the distribution of phthalates in the air and dust: a global scenario. Science of the Total Environment, 635, 817-827. https://doi.org/10.1016/j.scitotenv.2018.04.158
Kim, B., Lee, J.S., Choi, B.S., Park, S.Y., Yoon, J.H. & Kim, H. (2013) Ultrafine particle characteristics in a rubber manufacturing factory. The Annals of Occupational Hygiene, 57(6), 728-739. https://doi.org/10.1093/annhyg/mes102
Kim, J.H. (2019) Di(2-ethylhexyl) phthalate promotes lung cancer cell line A549 progression via Wnt/beta-catenin signaling. The Journal of Toxicological Sciences, 44(4), 237-244. https://doi.org/10.2131/jts.44.237
Kirsch-Volders, M. & Fenech, M. (2001) Inclusion of micronuclei in non-divided mononuclear lymphocytes and necrosis/apoptosis may provide a more comprehensive cytokinesis block micronucleus assay for biomonitoring purposes. Mutagenesis, 16(1), 51-58. https://doi.org/10.1093/mutage/16.1.51
Kleinsasser, N.H., Kastenbauer, E.R., Weissacher, H., Muenzenrieder, R.K. & Harreus, U.A. (2000) Phthalates demonstrate genotoxicity on human mucosa of the upper aerodigestive tract. Environmental and Molecular Mutagenesis, 35(1), 9-12. https://doi.org/10.1002/(sici)1098-2280(2000)35:1<9::aid-em2>3.0.co;2-1
Kleinsasser, N.H., Wallner, B.C., Kastenbauer, E.R., Weissacher, H. & Harreus, U.A. (2001) Genotoxicity of di-butyl-phthalate and di-iso-butyl-phthalate in human lymphocytes and mucosal cells. Teratogenesis, Carcinogenesis, and Mutagenesis, 21(3), 189-196. https://doi.org/10.1002/tcm.1007
Kocbach Bolling, A., Holme, J.A., Bornehag, C.G., Nygaard, U.C., Bertelsen, R.J., Nånberg, E. et al. (2013) Pulmonary phthalate exposure and asthma-is PPAR a plausible mechanistic link? EXCLI Journal, 12, 733-759.
Kotha, S.R., Gurney, T., Magalang, M., Hund, T., Satoskar, A. & Mohler, P. (2014) Mitochondrial lipid peroxidation in lung damage and disease. In: Natarajan, V. & Parinandi, N. (Eds.) Respiratory medicine, Vol. 15. New York: Humana Press.
Kruger, T., Long, M. & Bonefeld-Jorgensen, E.C. (2008) Plastic components affect the activation of the aryl hydrocarbon and the androgen receptor. Toxicology, 246(2-3), 112-123. https://doi.org/10.1016/j.tox.2007.12.028
Kuo, P.L., Hsu, Y.L., Huang, M.S., Tsai, M.J. & Ko, Y.C. (2011) Ginger suppresses phthalate ester-induced airway remodeling. Journal of Agricultural and Food Chemistry, 59(7), 3429-3438. https://doi.org/10.1021/jf1049485
Lenz, A.G., Karg, E., Lentner, B., Dittrich, V., Brandenberger, C., Rothen-Rutishauser, B. et al. (2009) A dose-controlled system for air-liquid interface cell exposure and application to zinc oxide nanoparticles. Particle and Fibre Toxicology, 6, 32. https://doi.org/10.1186/1743-8977-6-32
Lenz, A.G., Stoeger, T., Cei, D., Schmidmeir, M., Semren, N., Burgstaller, G. et al. (2014) Efficient bioactive delivery of aerosolized drugs to human pulmonary epithelial cells cultured in air-liquid interface conditions. American Journal of Respiratory Cell and Molecular Biology, 51(4), 526-535. https://doi.org/10.1165/rcmb.2013-0479OC
Mateos, R., Goya, L. & Bravo, L. (2004) Determination of malondialdehyde by liquid chromatography as the 2,4-dinitrophenylhydrazone derivative: a marker for oxidative stress in cell cultures of human hepatoma HepG2. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences, 805(1), 33-39. https://doi.org/10.1016/j.jchromb.2004.02.004
Niedernhofer, L.J., Daniels, J.S., Rouzer, C.A., Greene, R.E. & Marnett, L.J. (2003) Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells. The Journal of Biological Chemistry, 278(33), 31426-31433. https://doi.org/10.1074/jbc.M212549200
Ninomiya, H., Nomura, K., Satoh, Y., Okumura, S., Nakagawa, K., Fujiwara, M. et al. (2006) Genetic instability in lung cancer: concurrent analysis of chromosomal, mini- and microsatellite instability and loss of heterozygosity. British Journal of Cancer, 94(10), 1485-1491. https://doi.org/10.1038/sj.bjc.6603121
Nitschke L, Breuer D, Frenzen A, Heinrich, B., Hebisch, R., Brock, T.H, et al. (2017) Phthalates-Method for the determination of phthalates in workplace air using gas chromatography mass spectrometry (GC-MS) [Phthalate - Methode zur Bestimmung von Phthalaten in der Luft am Arbeitsplatz mittels Gaschromatographie-Massenspektrometrie (GC-MS)] Air Monitoring Methods in German language Phthalate - Methode zur Bestimmung von Phthalaten in der Luft am Arbeitsplatz mittels Gaschromatographie-Massenspektrometrie (GC-MS). The MAK Collection for Occupational Health and Safety 2:1091-1111 doi:https://doi.org/10.1002/3527600418.am8461d0019
OECD. (2016) Guidelines for the testing of chemicals, in vitro mammalian cell micronucleus test no. 487. Section 4: health effects. Paris: OECD Publishing. https://doi.org/10.1787/20745788
Oesch, F., Fabian, E. & Landsiedel, R. (2019) Xenobiotica-metabolizing enzymes in the lung of experimental animals, man and in human lung models. Archives of Toxicology, 93(12), 3419-3489. https://doi.org/10.1007/s00204-019-02602-7
Rafael-Vazquez, L., Garcia-Trejo, S., Aztatzi-Aguilar, O.G., Bazan-Perkins, B. & Quintanilla-Vega, B. (2018) Exposure to diethylhexyl phthalate (DEHP) and monoethylhexyl phthalate (MEHP) promotes the loss of alveolar epithelial phenotype of A549 cells. Toxicology Letters, 294, 135-144. https://doi.org/10.1016/j.toxlet.2018.05.012
Rosefort, C., Fauth, E. & Zankl, H. (2004) Micronuclei induced by aneugens and clastogens in mononucleate and binucleate cells using the cytokinesis block assay. Mutagenesis, 19(4), 277-284. https://doi.org/10.1093/mutage/geh028
Sapkota, M. & Wyatt, T.A. (2015) Alcohol, aldehydes, adducts and airways. Biomolecules, 5(4), 2987-3008. https://doi.org/10.3390/biom5042987
Shi, Q., Tang, J., Wang, L., Liu, R. & Giesy, J.P. (2021) Combined cytotoxicity of polystyrene nanoplastics and phthalate esters on human lung epithelial A549 cells and its mechanism. Ecotoxicology and Environmental Safety, 213, 112041. https://doi.org/10.1016/j.ecoenv.2021.112041
Sicinska, P., Mokra, K., Wozniak, K., Michalowicz, J. & Bukowska, B. (2021) Genotoxic risk assessment and mechanism of DNA damage induced by phthalates and their metabolites in human peripheral blood mononuclear cells. Scientific Reports, 11(1), 1658. https://doi.org/10.1038/s41598-020-79932-5
Szewczyńska, M., Pośniak, M. & Dobrzyńska, E. (2020) Determination of phthalates in particulate matter and gaseous phase emitted into the air of the working environment. International Journal of Environmental Science and Technology, 17(1735-1472), 175-186. https://doi.org/10.1007/s13762-019-02435-y
Theriault, M., Yoeuth, S., Matar, J., Martin, J., Bello, D. & Barry, C. (2017) Investigation of nanoparticles emitted when injection molding neat and additive-filled polypropylene and polycarbonate. AIP Conference Proceedings, 1914(1), 140008. https://doi.org/10.1063/1.5016773
Wang, Q., Cai, C., Wang, M., Guo, Q., Wang, B., Luo, W. et al. (2018) Efficient Photocatalytic degradation of malachite green in seawater by the hybrid of zinc-oxide Nanorods grown on three-dimensional (3D) reduced Graphene oxide(RGO)/Ni foam. Materials (Basel), 11(6), 1004. https://doi.org/10.3390/ma11061004
Wang, Y., Zhu, H. & Kannan, K. (2019) A review of biomonitoring of phthalate exposures. Toxics, 7(2), 21. https://doi.org/10.3390/toxics7020021
Wang, Y.C., Chen, H.S., Long, C.Y., Tsai, C.F., Hsieh, T.H., Hsu, C.Y. et al. (2012) Possible mechanism of phthalates-induced tumorigenesis. The Kaohsiung Journal of Medical Sciences, 28(7 Suppl), S22-S27. https://doi.org/10.1016/j.kjms.2012.05.006
Warner, G.R. & Flaws, J.A. (2018) Bisphenol a and phthalates: how environmental chemicals are reshaping toxicology. Toxicological Sciences, 166(2), 246-249. https://doi.org/10.1093/toxsci/kfy232
Wei, W., Ramalho, O. & Mandin, C. (2020) Modeling the bioaccessibility of inhaled semivolatile organic compounds in the human respiratory tract. International Journal of Hygiene and Environmental Health, 224, 113436. https://doi.org/10.1016/j.ijheh.2019.113436
Wojtowicz, A.K., Szychowski, K.A., Wnuk, A. & Kajta, M. (2017) Dibutyl phthalate (DBP)-induced apoptosis and neurotoxicity are mediated via the aryl hydrocarbon receptor (AhR) but not by estrogen receptor alpha (ERalpha), estrogen receptor beta (ERbeta), or peroxisome proliferator-activated receptor gamma (PPARgamma) in mouse cortical neurons. Neurotoxicity Research, 31(1), 77-89. https://doi.org/10.1007/s12640-016-9665-x
Wu, X., Lintelmann, J., Klingbeil, S., Li, J., Wang, H., Kuhn, E. et al. (2017) Determination of air pollution-related biomarkers of exposure in urine of travellers between Germany and China using liquid chromatographic and liquid chromatographic-mass spectrometric methods: a pilot study. Biomarkers, 22(6), 525-536. https://doi.org/10.1080/1354750X.2017.1306753
Wypych, A. (2017) Databook of plastiziers, 2nd edition. Canada: Elsevier, ChemTec Publishing, pp. 435-560. https://doi.org/10.1016/B978-1-895198-96-6.50028-6
Zoeller, R.T., Brown, T.R., Doan, L.L., Gore, A.C., Skakkebaek, N.E., Soto, A.M. et al. (2012) Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology, 153(9), 4097-4110. https://doi.org/10.1210/en.2012-1422

Auteurs

Stephanie Binder (S)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.
Joint Mass Spectrometry Center at Analytical Chemistry, Institute of Chemistry, University of Rostock, Rostock, Germany.

Xin Cao (X)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.
Joint Mass Spectrometry Center at Analytical Chemistry, Institute of Chemistry, University of Rostock, Rostock, Germany.

Stefanie Bauer (S)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Narges Rastak (N)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Evelyn Kuhn (E)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

George C Dragan (GC)

Federal Institute for Occupational Safety and Health (BAuA) - Measurement of Hazardous Substances, Dortmund, Germany.

Christian Monsé (C)

Institute for Prevention and Occupational Medicine of the German Social Accident Insurance (IFA), Institute of the Ruhr-Universität Bochum (IPA), Bochum, Germany.

George Ferron (G)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Dietmar Breuer (D)

Institute of Occupational Safety of the German Social Accident Insurance (IFA), Sankt Augustin, Germany.

Sebastian Oeder (S)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Erwin Karg (E)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Martin Sklorz (M)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Sebastiano Di Bucchianico (S)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.

Ralf Zimmermann (R)

Joint Mass Spectrometry Center at Comprehensive Molecular Analytics, Helmholtz Zentrum München, Neuherberg, Germany.
Joint Mass Spectrometry Center at Analytical Chemistry, Institute of Chemistry, University of Rostock, Rostock, Germany.

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