Oxidative Potential, Cytotoxicity, and Intracellular Oxidative Stress Generating Capacity of PM10: A Case Study in South of Italy
Abstract
:1. Introduction
2. Methods
2.1. Collection and Treatment of Samples
2.2. OC, EC, and TC Measurement
2.3. Determination of OP with DTT Assay
2.4. Cell Viability Measurement by MTT Assay
2.5. Intracellular Oxidative Stress Detection
2.6. Comet Assay for Genotoxicity Assessment
3. Results and Discussion
3.1. PM10 Oxidative Potential
3.2. PM10 Cytotoxicity
3.3. Intracellular Oxidative Stress Induction by PM10 Exposure
3.4. Correlation of OP, Cytotoxicity, and Oxidative Stress Generating Capacity of PM10 with Particulate Concentration and Carbon Content
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Anderson, J.O.; Thundiyil, J.G.; Stolbach, A. Clearing the air: A review of the effects of particulate matter air pollution on human health. JMT 2012, 8, 166–175. [Google Scholar] [CrossRef] [Green Version]
- Liu, S.; Zhou, Y.; Liu, S.; Chen, X.; Zou, W.; Zhao, D.; Li, X.; Pu, J.; Huang, L.; Chen, J.; et al. Association between exposure to ambient particulate matter and chronic obstructive pulmonary disease: Results from a cross-sectional study in China. Thorax 2017, 72, 788–795. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Loomis, D.; Grosse, Y.; Lauby-Secretan, B.; Ghissassi, F.E.; Bouvard, V.; Benbrahim-Tallaa, L.; Guha, N.; Baan, R.; Mattock, H.; Straif, K. International Agency for Research on Cancer Monograph Working Group IARC. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013, 14, 1262–1263. [Google Scholar] [CrossRef]
- Amato, F.; Alastuey, A.; Karanasiou, A.; Lucarelli, F.; Nava, S.; Calzolai, G.; Severi, M.; Becagli, S.; Vorne, L.G.; Colombi, C.; et al. AIRUSE-LIFEC: A harmonized PM speciation and source apportionment in five southern European cities. Atmos. Chem. Phys. 2016, 16, 3289–3309. [Google Scholar] [CrossRef] [Green Version]
- Li, N.; Sioutas, C.; Cho, A.; Schmitz, D.; Misra, C.; Sempf, J.; Wang, M.; Oberley, T.; Froines, J.; Nel, A. Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ. Health Perspect. 2003, 111, 455–460. [Google Scholar] [CrossRef] [PubMed]
- Jia, Y.Y.; Wang, Q.; Liu, T. Toxicity Research of PM2.5 Compositions in Vitro. Int. J. Environ. Res. Public Health 2017, 14, 232. [Google Scholar] [CrossRef] [Green Version]
- Nel, A. Air pollution related illness: Effects of particles. Science 2005, 308, 804–806. [Google Scholar] [CrossRef]
- Cheng, H.; Saffari, A.; Sioutas, C.; Forman, H.J.; Morgan, T.E.; Finch, C.E. Nanoscale particulate matter from urban traffic rapidly induces oxidative stress and inflammation in olfactory epithelium with concomitant effects on brain. Environ. Health Perspect. 2016, 124, 1537–1546. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sies, H. Oxidative stress: A concept in redox biology and medicine. Redox Biol. 2015, 4, 180–183. [Google Scholar] [CrossRef] [Green Version]
- Leomanni, A.; Schettino, T.; Calisi, A.; Gorbi, S.; Mezzelani, M.; Regoli, F.; Lionetto, M.G. Antioxidant and oxidative stress related responses in the Mediterranean land snail Cantareus apertus exposed to the carbamate pesticide Carbaryl. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2015, 168, 20–27. [Google Scholar] [CrossRef]
- Ayres, J.G.; Borm, P.; Cassee, F.R.; Castranova, V.; Donaldson, K.; Ghio, A.; Harrison, R.M.; Hider, R.; Kelly, F.; Kooter, I.M.; et al. Evaluating the toxicity of airborne particulate matter and nanoparticles by measuring oxidative stress potential—A Workshop report and consensus statement. Inhal. Toxicol. 2008, 20, 75–99. [Google Scholar] [CrossRef]
- Xiao, G.G.; Wang, M.; Li, N.; Loo, J.A.; Nel, A.E. Use of proteomics to demonstrate a hierarchical oxidative stress responseto diesel exhaust particles in a macrophage cell line. J. Biol. Chem. 2003, 278, 50781–50790. [Google Scholar] [CrossRef] [Green Version]
- Jiang, H.; Ahmed, C.M.S.; Canchola, A.; Chen, J.Y.; Lin, Y.H. Use of Dithiothreitol Assay to Evaluate the Oxidative Potential of Atmospheric Aerosols. Atmosphere 2019, 10, 571. [Google Scholar] [CrossRef] [Green Version]
- Ghio, A.J.; Carraway, M.S.; Madden, M.C. Composition of air pollution particles and oxidative stress in cells, tissues, and living systems. J. Toxicol. Environ. Health B Crit. Rev. 2012, 15, 1–21. [Google Scholar] [CrossRef]
- Bates, J.T.; Fang, T.; Verma, V.; Zeng, L.; Weber, R.J.; Tolbert, P.E.; Abrams, J.Y.; Sarnat, S.E.; Klein, M.; Mulholland, J.A.; et al. Review of acellular assays of ambient particulate matter oxidative potential: Methods and relationships with composition, sources, and health effects. Environ. Sci. Technol. 2019, 53, 4003–4019. [Google Scholar] [CrossRef]
- Lionetto, M.G.; Guascito, M.R.; Caricato, R.; Giordano, M.E.; De Bartolomeo, A.R.; Romano, M.P.; Conte, M.; Dinoi, A.; Contini, D. Correlation of Oxidative Potential with Ecotoxicological and Cytotoxicological Potential of PM10 at an Urban Background Site in Italy. Atmosphere 2019, 10, 733. [Google Scholar] [CrossRef] [Green Version]
- Shi, T.; Schins, R.P.F.; Knaapen, A.M.; Kuhlbusch, T.; Pitz, M.; Heinrich, J.; Borm, P.J.A. Hydroxyl radical generation by election paramagnetic resonance as a new method to monitor ambient particulate matter composition. J. Environ. Monit. 2003a, 5, 550–556. [Google Scholar] [CrossRef]
- Shi, T.; Knaapen, A.M.; Begerow, J.; Birmilli, W.; Borm, P.J.A.; Schins, R.P.F. Temporal variation of hydroxyl radical generation and 8-hydroxy-2′-deoxyguanosine formation by coarse and fine particulate matter. Occup. Environ. Med. 2003b, 60, 315–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mudway, I.; Fuller, G.W.; Green, D.; Dunster, C.; Kelly, F.J. Quantifying the London Specific Component of PM10 Oxidative Activity; Report Defra Department of Environmental Food and Rural Affairs; DEFRA: London, UK, 2011. [Google Scholar]
- Cho, A.K.; Sioutas, C.; Miguel, A.H.; Kumagai, Y.; Schmitz, D.A.; Singh, M.; Eiguren-Fernandez, A.; Froines, J.R. Redox activity of airborne particulate matter at different sites in the Los Angeles Basin. Environ. Res. 2005, 99, 40–47. [Google Scholar] [CrossRef] [PubMed]
- Hiura, T.S.; Li, N.; Kaplan, R.; Horwitz, M.; Seagrave, J.C.; Nel, A.E. The role of a mitochondrial pathway in the induction of apoptosis by chemicals extracted from diesel exhaust particles. J. Immunol. 2000, 165, 2703–2711. [Google Scholar] [CrossRef] [Green Version]
- Crobeddu, B.; Aragao-Santiago, L.; Bui, L.C.; Boland, S.; Squiban, A.B. Oxidative potential of particulate matter 2.5 as predictive indicator of cellular stress. Environ. Pollut. 2017, 230, 125–133. [Google Scholar]
- Daellenbach, K.R.; Uzu, G.; Jiang, J.; Cassagnes, L.-E.; Leni, Z.; Vlachou, A.; Stefenelli, G.; Canonaco, F.; Weber, S.; Segers, A.; et al. Sources of particulate-matter air pollution and its oxidative potential in Europe. Nature 2020, 587, 414–419. [Google Scholar] [CrossRef]
- Øvrevik, J. Oxidative Potential Versus Biological Effects: A Review on the Relevance of Cell-Free/Abiotic Assays as Predictors of Toxicity from Airborne Particulate Matter. Int. J. Mol. Sci. 2019, 20, 4772. [Google Scholar] [CrossRef] [Green Version]
- Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55–63. [Google Scholar] [CrossRef]
- Hsiao, W.L.W.; Moa, Z.Y.; Fang, M.; Shi, X.M.; Wang, F. Cytotoxicity of PM2.5 and PM2.5–10 ambient air pollutants assessed by the MTT and the Comet assays. Mutat. Res. 2000, 471, 45–55. [Google Scholar] [CrossRef]
- Faraji, M.; Nodehi, R.N.; Naddafi, K.; Pourpak, Z.; Alizadeh, Z.; Rezaei, S.; Mesdaghinia, A. Cytotoxicity of airborne particulate matter (PM10) from dust storm and inversion conditions assessed by MTT assay. J. Air Pollut. Health 2018, 3, 135–142. [Google Scholar]
- Arto, S.; Sillanpaa, M.; Halinen, A.I.; Happo, M.S.; Hillamo, R.; Brunekreef, B.; Katsouyanni, K.; Sunyer, J.; Hirvonen, M.R. Heterogeneities in inflammatory and cytotoxic responses of RAW 264.7 macrophage cell line to urban air coarse, fine, and ultrafine particles from six European sampling campaigns. Inhal. Toxicol. 2007, 19, 213–225. [Google Scholar]
- Singh, N.P.; McCoy, M.T.; Tice, R.R.; Schneider, E.L. A simple technique for quantification of low levels of DNA damage in individual cells. Exp. Cell. Res. 1988, 175, 184–189. [Google Scholar] [CrossRef] [Green Version]
- Collins, A.R. The Comet Assay-principles, applications and limitations. Methods Mol. Biol. 2003, 203, 163–167. [Google Scholar]
- Foster, K.A.; Oster, C.G.; Mayer, M.M.; Avery, M.L.; Audus, K.L. Characterization of the A549 Cell Line as a Type II Pulmonary Epithelial Cell Model for Drug Metabolism. Exp. Cell Res. 1998, 243, 359–366. [Google Scholar] [CrossRef]
- Yi, S.; Zhang, F.; Qu, F.; Ding, W. Water-insoluble fraction of airborne particulate matter (PM10) induces oxidative stress in human lung epithelial A549 cells. Environ. Toxicol. 2012, 29, 226–233. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Li, K.; Jin, W.; Lu, Y.; Zhang, Y.; Shen, G.; Wang, R.; Shen, H.; Li, W.; Huang, Y.; et al. Properties and Inflammatory Effects of Various Size Fractions of Ambient Particulate Matter from Beijing on A549 and J774A.1 Cells. Environ. Sci. Technol. 2013, 47, 10583–10590. [Google Scholar] [CrossRef]
- Cesari, D.; Merico, E.; Dinoi, A.; Marinoni, A.; Bonasoni, P.; Contini, D. Seasonal variability of carbonaceous aerosols in an urban background area in Southern Italy. Atmos. Res. 2018, 200, 97–108. [Google Scholar] [CrossRef]
- Dinoi, A.; Cesari, D.; Marinoni, A.; Bonasoni, P.; Riccio, A.; Chianese, E.; Tirimberio, G.; Naccarato, A.; Sprovieri, F.; Andreoli, G.; et al. Inter-Comparison of Carbon Content in PM2.5 and PM10 Collected at Five Measurement Sites in Southern Italy. Atmosphere 2017, 8, 243. [Google Scholar] [CrossRef] [Green Version]
- Conte, M.; Merico, E.; Cesari, D.; Dinoi, A.; Grasso, F.M.; Donateo, A.; Guascito, M.R.; Contini, D. Long-term characterisation of African dust advection in south-eastern Italy: Influence on fine and coarse particle concentrations, size distributions, and carbon content. Atmos. Res. 2020, 233, 104690. [Google Scholar] [CrossRef]
- Merico, E.; Cesari, D.; Dinoi, A.; Gambaro, A.; Barbaro, E.; Guascito, M.R.; Giannossa, L.C.; Mangone, A.; Contini, D. Inter-comparison of carbon content in PM10 and PM2.5 measured with two thermo-optical protocols on samples collected in a Mediterranean site. Environ. Sci. Pollut. Res. 2019, 26, 29334–29350. [Google Scholar] [CrossRef] [PubMed]
- Chirizzi, D.; Cesari, D.; Guascito, M.R.; Dinoi, A.; Giotta, L.; Donateo, A.; Contini, D. Influence of Saharan dust outbreaks and carbon content on oxidative potential of water-soluble fractions of PM2.5 and PM10. Atmos. Environ. 2017, 163, 1–8. [Google Scholar] [CrossRef]
- Latronico, S.; Giordano, M.E.; Urso, E.; Lionetto, M.G.; Schettino, T. Effect of the flame retardant Tris (1,3-dichloro-2-propyl) Phosphate (TDCPP) on Na+-K+-ATPase and Cl- transport in HeLa cells. Toxicol. Mech. Methods 2018, 28, 599–606. [Google Scholar] [CrossRef]
- Forman, H.J.; Augusto, O.; Brigelius-Flohe, R.; Dennery, P.A.; Kalyanaraman, B.; Ischiropoulos, H.; Mann, G.E.; Radi, R.; RobertsII, L.J.; Vina, J.; et al. Even free radicals should follow some rules: A Guide to free radical research terminology and methodology. Free Radic. Biol. Med. 2015, 78, 233–235. [Google Scholar] [CrossRef] [PubMed]
- Giordano, M.E.; Caricato, R.; Lionetto, M.G. Concentration dependence of the antioxidant and prooxidant activity of Trolox in HeLa cells: Involvement in the induction of Apoptotic Volume Decrease. Antioxidants 2020, 9, 1058. [Google Scholar] [CrossRef]
- Contini, D.; Genga, A.; Cesari, D.; Siciliano, M.; Donateo, A.; Bove, M.C.; Guascito, M.R. Characterisation and source apportionment of PM10 in an urban background site in Lecce. Atmos. Res. 2010, 95, 40–54. [Google Scholar] [CrossRef]
- Contini, D.; Cesari, D.; Donateo, A.; Chirizzi, D.; Belosi, F. Characterization of PM10 and PM2.5 and Their Metals Content in Different Typologies of Sites in South-Eastern Italy. Atmosphere 2014, 5, 435–453. [Google Scholar] [CrossRef] [Green Version]
- Romano, S.; Perrone, M.R.; Becagli, S.; Pietrogrande, M.C.; Russo, M.; Caricato, R.; Lionetto, M.G. Ecotoxicity, genotoxicity, and oxidative potential tests of atmospheric PM10 particles. Atmos. Environ. 2020, 221, 117085. [Google Scholar] [CrossRef]
- Sandrini, S.; Fuzzi, S.; Piazzalunga, A.; Prati, P.; Bonasoni, P.; Cavalli, F.; Bove, M.C.; Calvello, M.; Cappelletti, D.; Colombi, C.; et al. Spatial and seasonal variability of carbonaceous aerosol across Italy. Atmos. Environ. 2014, 99, 587–598. [Google Scholar] [CrossRef]
- Cesari, D.; Donateo, A.; Conte, M.; Merico, E.; Giangreco, A.; Giangreco, F.; Contini, D. An inter-comparison of PM2.5 at urban and urban background sites: Chemical characterization and source apportionment. Atmos. Res. 2016, 174–175, 106–119. [Google Scholar] [CrossRef]
- Janssen, N.A.H.; Yang, A.; Strak, M.; Steenhof, M.; Hellack, B.; Gerlofs-Nijland, M.E.; Kuhlbusch, T.; Kelly, F.; Harrison, R.; Brunekreef, B.; et al. Oxidative potential of particulate matter collected at sites with different source characteristics. Sci. Total Environ. 2014, 472, 572–581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cesari, D.; Merico, E.; Grasso, F.M.; Decesari, S.; Belosi, F.; Manarini, F.; De Nuntiis, P.; Rinaldi, M.; Volpi, F.; Gambaro, A.; et al. Source apportionment of PM2.5 and of its oxidative potential in an industrial suburban site in south Italy. Atmosphere 2019, 10, 758. [Google Scholar] [CrossRef] [Green Version]
- Perrone, M.R.; Bertoli, I.; Romano, S.; Russo, M.; Rispoli, G.; Pietrogrande, M.C. PM2.5 and PM10 oxidative potential at a Central Mediterranean Site: Contrasts between dithiothreitol-and ascorbic acid-measured values in relation with particle size and chemical composition. Atmos. Environ. 2019, 210, 143–155. [Google Scholar] [CrossRef]
- Pietrogrande, M.C.; Russo, M.; Zagatti, E. Review of PM oxidative potential measured with acellular assays in urban and rural sites across Italy. Atmosphere 2020, 10, 626. [Google Scholar] [CrossRef] [Green Version]
- Massimi, L.; Ristorini, M.; Simonetti, G.; Frezzini, M.A.; Astolfi, M.L.; Canepari, S. Spatial mapping and size distribution of oxidative potential of particulate matter released by spatially disaggregated sources. Environ. Pollut. 2020, 266, 115271. [Google Scholar] [CrossRef]
- Voelkel, K.; Krug, H.F.; Diabate, S. Formation of reactive oxygen species in rat epithelial cells upon stimulation with fly ash. J. Biosci. 2003, 28, 51–55. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Wang, Y.; Qiu, X.; Xu, F.; Chen, R.; Gu, W.; Zhang, L.; Yang, S.; Cai, Z.; Liu, C. Difference on oxidative stress in lung epithelial cells and macrophages induced by ambient fine particulate matter (PM2.5). Air Qual. Atmos. Health 2020, 13, 789–796. [Google Scholar] [CrossRef]
- Kampfrath, T.; Maiseyeu, A.; Ying, Z.; Shah, Z.; Deiuliis, J.A.; Xu, X.; Kherada, N.; Brook, R.D.; Reddy, K.M.; Padture, N.P.; et al. Chronic fine particulate matter exposure induces systemic vascular dysfunction via NADPH oxidase and TLR4 pathways. Circ. Res. 2011, 108, 716–726. [Google Scholar] [CrossRef] [Green Version]
- Xu, X.; Yavar, Z.; Verdin, M.; Ying, Z.; Mihai, G.; Kampfrath, T.; Wang, A.; Zhing, M.; Lippermann, M.; Chen, L.C.; et al. Effect of early particulate air pollution exposure on obesity in mice: Role of p47phox. Arterioscler. Thromb. Vasc. Biol. 2010, 30, 2518–2527. [Google Scholar] [CrossRef] [Green Version]
- Imlay, J.A.; Chin, S.M.; Linn, S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988, 240, 640–642. [Google Scholar] [CrossRef] [PubMed]
- Xia, T.; Korge, P.; Weiss, J.N.; Li, N.; Venkatesen, M.I.; Sioutas, C.; Nel, A. Quinones and aromatic chemical compounds in particulate matter induce mitochondrial dysfunction: Implications for ultrafine particle toxicity. Environ. Health Perspect. 2004, 112, 1347–1358. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez-Hunt, C.P.; Wadhwa, M.; Sanders, L.H. DNA damage by oxidative stress: Measurement strategies for two genomes. Curr. Opin. Toxicol. 2018, 7, 87–94. [Google Scholar] [CrossRef]
- Packer, P.; Beckman, J.S.; Liaudet, L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87, 315–424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Park, M.; Joo, H.S.; Lee, K.; Jang, M.; Kim, S.D.; Kim, I.; Borlaza, L.J.S.; Lim, H.; Shin, H.; Chung, K.H.; et al. Differential toxicities of fine particulate matters from various sources. Sci. Rep. 2018, 8, 17007. [Google Scholar] [CrossRef]
- Wang, Y.; Plewab, M.J.; Mukherjee, U.K.; Verma, V. Assessing the cytotoxicity of ambient particulate matter (PM) using Chinese hamster ovary (CHO) cells and its relationship with the PM chemical composition and oxidative potential. Atmos. Environ. 2018, 179, 132–141. [Google Scholar] [CrossRef]
PM10 (µg/m3) | OC (µg/m3) | EC (µg/m3) | TC (µg/m3) | MTT (% inhibition) | OPDDTV (nmol/min*m3) | OPDDTM (pmol/min*µg) | |
---|---|---|---|---|---|---|---|
Average | 21.0 | 3.4 | 0.7 | 4.0 | 21.8 | 0.3 | 14.2 |
(min-max) | (5.5–42.4) | (0.9–13.8) | (0.1–2.0) | (1.2–15.8) | (5.3–81.6) | (0.1–0.7) | (4.9–23.9) |
Median | 19.5 | 2.7 | 0.6 | 4.0 | 20.2 | 0.3 | 15.0 |
(25th–75th) | (14.5–26.1) | (1.8–4.1) | (0.3–0.8) | (2.2–4.8) | (11.3–29.2) | (0.2–0.3) | (10.3–17.0) |
PM10 (µg/m3) | OC (µg/m3) | EC (µg/m3) | TC (µg/m3) | N of Pairs | |
---|---|---|---|---|---|
OPDTTV | 0.6843 ** | 0.8209 ** | 0.8179 ** | 0.8274 ** | 28 |
OPDTTM | −0.1679 | 0.2042 | 0.3387 | 0.2241 | 28 |
MTTV | 0.4545 | 0.8708 ** | 0.8304 ** | 0.8715 ** | 28 |
MTTM | −0.4765 | 0.2838 | 0.2946 | 0.2871 | 28 |
OSGCV | 0.5443 ** | 0.6477 ** | 0.7223 ** | 0.6631 ** | 28 |
OSGCM | −0.3877 | 0.0464 | 0.1674 | 0.0631 | 28 |
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Lionetto, M.G.; Guascito, M.R.; Giordano, M.E.; Caricato, R.; De Bartolomeo, A.R.; Romano, M.P.; Conte, M.; Dinoi, A.; Contini, D. Oxidative Potential, Cytotoxicity, and Intracellular Oxidative Stress Generating Capacity of PM10: A Case Study in South of Italy. Atmosphere 2021, 12, 464. https://doi.org/10.3390/atmos12040464
Lionetto MG, Guascito MR, Giordano ME, Caricato R, De Bartolomeo AR, Romano MP, Conte M, Dinoi A, Contini D. Oxidative Potential, Cytotoxicity, and Intracellular Oxidative Stress Generating Capacity of PM10: A Case Study in South of Italy. Atmosphere. 2021; 12(4):464. https://doi.org/10.3390/atmos12040464
Chicago/Turabian StyleLionetto, Maria Giulia, Maria Rachele Guascito, Maria Elena Giordano, Roberto Caricato, Anna Rita De Bartolomeo, Maria Pia Romano, Marianna Conte, Adelaide Dinoi, and Daniele Contini. 2021. "Oxidative Potential, Cytotoxicity, and Intracellular Oxidative Stress Generating Capacity of PM10: A Case Study in South of Italy" Atmosphere 12, no. 4: 464. https://doi.org/10.3390/atmos12040464