Effect of Atmospheric Aging on Soot Particle Toxicity in Lung Cell Models at the Air–Liquid Interface: Differential Toxicological Impacts of Biogenic and Anthropogenic Secondary Organic Aerosols (SOAs)
Svenja Offer, Elena Hartner, Sebastiano Di Bucchianico, Christoph Bisig, Stefanie Bauer, Jana Pantzke, Elias J. Zimmermann, Xin Cao, Stefanie Binder, Evelyn Kuhn, Anja Huber, Seongho Jeong, Uwe Käfer, Patrick Martens, Arunas Mesceriakovas, Jan Bendl, Ramona Brejcha, Angela Buchholz, Daniella Gat, Thorsten Hohaus, Narges Rastak, Gert Jakobi, Markus Kalberer, Tamara Kanashova, Yue Hu, Christoph Ogris, Annalisa Marsico, Fabian Theis, Michal Pardo, Thomas Gröger, Sebastian Oeder, Jürgen Orasche, Andreas Paul, Till Ziehm, Zhi-Hui Zhang, Thomas Adam, Olli Sippula, Martin Sklorz, Jürgen Schnelle-Kreis, Hendryk Czech, Astrid Kiendler-Scharr, Yinon Rudich, Ralf Zimmermann
Abstract
Background: Secondary organic aerosols (SOAs) formed from anthropogenic or biogenic gaseous precursors in the atmosphere substantially contribute to the ambient fine particulate matter [PM ≤2.5μm in aerodynamic diameter (PM2.5)] burden, which has been associated with adverse human health effects. However, there is only limited evidence on their differential toxicological impact. Objectives: We aimed to discriminate toxicological effects of aerosols generated by atmospheric aging on combustion soot particles (SPs) of gaseous biogenic (β-pinene) or anthropogenic (naphthalene) precursors in two different lung cell models exposed at the air–liquid interface (ALI). Methods: Mono- or cocultures of lung epithelial cells (A549) and endothelial cells (EA.hy926) were exposed at the ALI for 4 h to different aerosol concentrations of a photochemically aged mixture of primary combustion SP and β-pinene (SOAβPIN-SP) or naphthalene (SOANAP-SP). The internally mixed soot/SOA particles were comprehensively characterized in terms of their physical and chemical properties. We conducted toxicity tests to determine cytotoxicity, intracellular oxidative stress, primary and secondary genotoxicity, as well as inflammatory and angiogenic effects. Results: We observed considerable toxicity-related outcomes in cells treated with either SOA type. Greater adverse effects were measured for SOANAP-SP compared with SOAβPIN-SP in both cell models, whereas the nano-sized soot cores alone showed only minor effects. At the functional level, we found that SOANAP-SP augmented the secretion of malondialdehyde and interleukin-8 and may have induced the activation of endothelial cells in the coculture system. This activation was confirmed by comet assay, suggesting secondary genotoxicity and greater angiogenic potential. Chemical characterization of PM revealed distinct qualitative differences in the composition of the two secondary aerosol types. Discussion: In this study using A549 and EA.hy926 cells exposed at ALI, SOA compounds had greater toxicity than primary SPs. Photochemical aging of naphthalene was associated with the formation of more oxidized, more aromatic SOAs with a higher oxidative potential and toxicity compared with β-pinene. Thus, we conclude that the influence of atmospheric chemistry on the chemical PM composition plays a crucial role for the adverse health outcome of emissions. https://doi.org/10.1289/EHP9413