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Importance of surface charge of soot nanoparticles in determining inhalation toxicity in mice

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Abstract

Physicochemical properties of nanoparticles are important in regulating nanoparticle toxicity; however, the contribution of nanoparticle charge remains unclear. The objective of this study was to investigate the pulmonary effects of inhalation of charged soot nanoparticles. We established a stably charged nanoparticle generation system for whole-body exposure in BALB/c mice, which produced positively charged, negatively charged, and neutral soot nanoparticles in a wide range of concentrations. After a 7-day exposure, pulmonary toxicity was assessed, together with proteomics analysis. The charged soot nanoparticles on average carried 1.17–1.35 electric charges, and the sizes for nanoparticles under different charging conditions were all fixed at 69 ~ 72 nm. We observed that charged soot nanoparticles induced cytotoxic LDH and increased lung permeability, with the release of 8-isoprostane and caspase-3 and systemic IL-6 in mice, especially for positively charged soot nanoparticles. Next, we observed that positive-charged soot nanoparticles upregulated Eif2, Eif4, sirtuin, mammalian target of rapamycin (mTOR), peroxisome proliferator-activated receptors (PPAR), and HIPPO-related signaling pathways in the lungs compared with negatively charged soot nanoparticles. HIF1α, sirt1, E-cadherin, and Yap were increased in mice’s lungs by positively charged soot nanoparticle exposure. In conclusion, carbonaceous nanoparticles carrying electric ions, especially positive-charged, are particularly toxic when inhaled and should be of concern in terms of pulmonary health protection.

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Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors wish to thank Miss Yi-Syuan Lin for the technical assistance of this research. The authors acknowledge the mass spectrometry technical research services of NTU Consortia of Key Technologies. KF Chung is a Visiting Professor at Taipei Medical University.

Funding

This study was funded by the Ministry of Science and Technology of Taiwan (109–2314-B-038–093-MY3, 110–2113-M-038–001-MY3, and 111–2314-B-038–079).

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Author notes

  1. Ta-Chih Hsiao and Chia-Li Han contributed equally to this work.

Authors and Affiliations

  1. Graduate Institute of Environmental Engineering, National Taiwan University, Taipei, Taiwan

    Ta-Chih Hsiao

  2. Master Program in Clinical Genomics and Proteomics, College of Pharmacy, Taipei Medical University, Taipei, Taiwan

    Chia-Li Han

  3. Department of Environmental Engineering and Health, Yuanpei University of Medical Technology, Hsin Chu City, Taiwan

    Tzu-Ting Yang

  4. Department of Microbiology and Immunology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Yueh-Lun Lee

  5. Graduate Institute of Environmental Engineering, National Center University, Tauyoun, Taiwan

    Yu-Fang Shen

  6. Genome and Systems Biology Degree Program, Academia Sinica and National Taiwan University, Taipei, Taiwan

    Yu-Teng Jheng

  7. Department of Pathology, Taipei City Hospital Heping Fuyou Branch, Taipei, Taiwan

    Chii-Hong Lee & Hsiao-Chi Chuang

  8. School of Respiratory Therapy, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Jer-Hwa Chang

  9. Division of Pulmonary Medicine, Department of Internal Medicine, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan

    Jer-Hwa Chang

  10. National Heart and Lung Institute, Imperial College London, London, UK

    Kian Fan Chung

  11. Division of Pulmonary Medicine, Department of Internal Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Han-Pin Kuo

  12. Division of Pulmonary Medicine, Department of Internal Medicine, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Hsiao-Chi Chuang

  13. Cell Physiology and Molecular Image Research Center, Wan Fang Hospital, Taipei Medical University, Taipei, Taiwan

    Hsiao-Chi Chuang

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  1. Ta-Chih Hsiao
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by TCH, CLH, TTY, YFS, YTJ, CHL YLL, and JHC. The first draft of the manuscript was written by TCH, KFC, HPK, and HCC, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hsiao-Chi Chuang.

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The animal study was performed in compliance with the animal and ethics review committee of the Laboratory Animal Center at Taipei Medical University (Taipei, Taiwan; LAC-2015–0017).

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Hsiao, TC., Han, CL., Yang, TT. et al. Importance of surface charge of soot nanoparticles in determining inhalation toxicity in mice. Environ Sci Pollut Res 30, 18985–18997 (2023). https://doi.org/10.1007/s11356-022-23444-4

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