Skip to main content

Advertisement

Springer Nature Link
Log in

The toxicological analysis of secondary organic aerosol in human lung epithelial cells and macrophages

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Secondary organic aerosol (SOA) is a component of airborne particulate matter in urban areas. However, their toxicities remain incompletely understood. In this study, we investigated the oxidative and inflammatory potency of SOA derived from three different volatile organic compounds (α-pinene, m-xylene, and trimethylbenzene) using human bronchial epithelial cells (BEAS-2B) and macrophages (U937). In BEAS-2B cells, all types of SOA extracts increased the expression of the heme oxygenase 1 (HMOX1) and interleukin-8 (IL8) genes, a typical marker for oxidative stress and inflammatory responses, respectively. Among the three types of SOA, m-xylene-derived SOA showed the strongest induction of the HMOX1 and IL8 genes, and transcriptional activity via the antioxidant response element (ARE). A causal candidate for SOA induction of oxidative stress is 2,6-dimethyl-1,4-benzoquinone (DMBQ) because only this quinone compound increased the transcriptional activity via ARE among components tested in this study. Similar to the case of BEAS-2B cells, SOA extracts increased the expression of HMOX1 and IL8 genes in U937 cells, mainly through oxidative stress, but these responses in U937 cells were prolonged when compared with BEAS-2B cells. Together, these results show that SOA affects lung epithelial cells and macrophages mainly through oxidative stress and inflammation, suggesting their contribution to the development of respiratory diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Andrè E, Campi B, Materazzi S, Trevisani M, Amadesi S, Massi D, Creminon C, Vaksman N, Nassini R, Civelli M, Baraldi PG, Poole DP, Bunnett NW, Geppetti P, Patacchini R (2008) Cigarette smoke-induced neurogenic inflammation is mediated by alpha,beta-unsaturated aldehydes and the TRPA1 receptor in rodents. J Clin Invest 118:2574–2582

    Google Scholar 

  • Bowler RP, Crapo JD (2002) Oxidative stress in allergic respiratory diseases. J Allergy Clin Immunol 110:349–356

    Article  CAS  Google Scholar 

  • Cho AK, Stefano ED, You Y, Rodriguez CE, Schmitz DA, Kumagai Y, Miguel AH, Eiguren-Fernandez A, Kobayashi T, Avol E, Froines JR (2004) Determination of four quinones in diesel exhaust particles, SRM 1649a, and atmospheric PM2.5. Aerosol Sci Technol 38:1–14

    Article  CAS  Google Scholar 

  • Docherty KS, Stone EA, Ulbrich IM, DeCarlo PF, Snyder DC, Chauer JJ, Peltier RE, Weber RJ, Murphy SM, Seinfeld JH, Grover BD, Eatough DJ, Jimenez JL (2008) Apportionment of primary and secondary organic aerosols in southern California during the 2005 study of organic aerosols in riverside (SOAR-1). Environ Sci Technol 42:7655–7662

    Article  CAS  Google Scholar 

  • Forstner HJL, Flagan RC, Seinfeld JH (1997) Secondary organic aerosol from the photooxidation of aromatic hydrocarbons: molecular composition. Environ Sci Technol 31:1345–1358

    Article  CAS  Google Scholar 

  • Fujitani Y, Sato K, Furuyama A, Fushimi A, Ito T, Tanabe K, Hirano S, Imamura T, Takami A (2012) Generation of secondary organic aerosols in a small chamber for toxicity studies. Earozoru Kenkyu 27:350–356

    CAS  Google Scholar 

  • Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M (2002) Multiple control of interleukin-8 gene expression. J Leukoc Biol 72:847–855

    CAS  Google Scholar 

  • Inoue K, Takano H, Ichinose T, Tomura S, Yanagisawa R, Sakurai M, Sumi D, Cho AK, Hiyoshi K, Kumagai Y (2007) Effects of naphthoquinone on airway responsiveness in the presence or absence of antigen in mice. Arch Toxicol 81:575–581

    Article  CAS  Google Scholar 

  • Klaunig JE, Kamendulis LM, Hocevar BA (2010) Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 38:96–102

    Article  CAS  Google Scholar 

  • Kondo Y, Miyazaki Y, Takegawa N, Miyakawa T, Weber RJ, Jimenez JL, Zhang Q, Worsnop DR (2007) Oxygenated and water-soluble organic aerosols in Tokyo. J Geophys Res 112:D01203. https://doi.org/10.1029/2006JD007056

    Article  CAS  Google Scholar 

  • Kroll JH, Seinfeld JH (2008) Chemistry of secondary organic aerosol: formation and evolution of low-volatility organics in the atmosphere. Atmos Environ 42:3593–3624

    Article  CAS  Google Scholar 

  • Kumagai Y, Arimoto T, Shinyashiki M, Shimojo N, Nakai Y, Yoshikawa T, Sagai M (1997) Generation of reactive oxygen species during interaction of diesel exhaust particle components with NAPDH-cytochrome P450 reductase and involvement of the bioactivation in the DNA damage. Free Radic Biol Med 22:479–487

    Article  CAS  Google Scholar 

  • Kumagai K, Iijima A, Tago H, Tomioka A, Kozawa K, Sakamoto K (2009) Seasonal characteristics of water-soluble organic carbon in atmospheric particles in the inland Kanto plain, Japan. Atmos Environ 43:3345–3351

    Article  CAS  Google Scholar 

  • Lechner JF, Haugen A, McClendon IA, Shamsuddin AM (1984) Induction of squamous differentiation of normal human bronchial epithelial cells by small amounts of serum. Differentiation 25:229–237

    Article  CAS  Google Scholar 

  • Li N, Alam J, Venkatesan MI, Eiguren-Fernandez A, Schmitz D, Di Stefano E, Slaughter N, Killeen E, Wang X, Huang A, Wang M, Miguel AH, Cho A, Sioutas C, Nel AE (2004) Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals. J Immunol 173:3467–3481

    Article  CAS  Google Scholar 

  • Michikawa T, Ueda K, Takeuchi A, Kinoshita M, Hayashi H, Ichinose T, Nitta H (2015) Impact of short-term exposure to fine particulate matter on emergency ambulance dispatches in Japan. J Epidemiol Community Health 69:86–91

    Article  Google Scholar 

  • Ofner J, Kruger HU, Grothe H, Schmitt-Lopplin P, Whitmore K, Zetzsch C (2011) Physico-chemical characterization of SOA derived from catechol and guaiacol - a model substance for the aromatic fraction of atmospheric HULIS. Atmos Chem Phys 11:1–15

    Article  CAS  Google Scholar 

  • Pankow JF (1994) An absorption model of the gas/aerosol, partitioning involved in the formation of secondary organic aerosol. Atmos Environ 28:189–193

    Article  CAS  Google Scholar 

  • Roy A, Hu W, Wei F, Korn L, Chapman RS, Zhang JJ (2012) Ambient particulate matter and lung function growth in Chinese children. Epidemiology 23:464–472

    Article  Google Scholar 

  • Sagai M, Saito H, Ichinose T, Kodama M, Mori Y (1993) Biological effects of diesel exhaust particles. I. In vitro production of superoxide and in vivo toxicity in mouse. Free Radic Biol Med 14:37–47

    Article  CAS  Google Scholar 

  • Schnabel R, Blankenberg S (2007) Oxidative stress in cardiovascular disease, successful translation from bench to bedside? Circulation 116:1338–1340

    Article  Google Scholar 

  • Sun Z, Huang Z, Zhang DD (2009) Phosphorylation of Nrf2 at multiple sites by MAP kinases has a limited contribution in modulating the Nrf2-depedent antioxidant response. PLoS One 4:e6588

    Article  CAS  Google Scholar 

  • Sunil VR, Laumbach RJ, Patel KJ, Turpin BJ, Lim HJ, Kipen HM, Laskin JD, Laskin DL (2007) Pulmonary effects of inhaled limonene ozone reaction products in elderly rats. Toxicol Appl Pharmacol 222:211–220

    Article  CAS  Google Scholar 

  • Taguchi K, Motohashi H, Yamamoto M (2011) Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16:123–140

    Article  CAS  Google Scholar 

  • Toriba A, Homma C, Kita M, Uozaki W, Boongla Y, Orakij W, Tang N, Kameda T, Hayakawa K (2016) Simultaneous determination of polycyclic aromatic hydrocarbon quinones by gas chromatography-tandem mass spectrometry, following a one-pot reductive trimethylsilyl derivatization. J Chromatogr A 1459:89–100

    Article  CAS  Google Scholar 

  • Wichmann HE, Peters A (2000) Epidemiological evidence of the effects of ultrafine particle exposure. Philos Trans R Soc Lond A 358:2751–2769

    Article  CAS  Google Scholar 

  • Zhang Y, Shu J, Zhang Y, Yang B (2013) Homogeneous and heterogeneous reactions of anthracene with selected atmospheric oxidants. J Environ Sci 25:1817–1823

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Ms. M. Ihara (National Institute for Environmental Studies) and Mr. T. Fujii (Horiba Techno Service) for their excellent technical assistance. We also thank A. Matsushima, M. Fujii, and M. Ikezawa for their secretary assistance.

Author information

Authors and Affiliations

  1. Center for Health and Environmental Risk Research, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki, 305-8506, Japan

    Tomohiro Ito, Kanae Bekki, Yuji Fujitani & Seishiro Hirano

Authors
  1. Tomohiro Ito
    View author publications

    Search author on:PubMed Google Scholar

  2. Kanae Bekki
    View author publications

    Search author on:PubMed Google Scholar

  3. Yuji Fujitani
    View author publications

    Search author on:PubMed Google Scholar

  4. Seishiro Hirano
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Tomohiro Ito.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ito, T., Bekki, K., Fujitani, Y. et al. The toxicological analysis of secondary organic aerosol in human lung epithelial cells and macrophages. Environ Sci Pollut Res 26, 22747–22755 (2019). https://doi.org/10.1007/s11356-019-05317-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05317-5

Keywords

Profiles

  1. Yuji Fujitani View author profile