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Early-life long-term exposure to ZnO nanoparticles suppresses innate immunity regulated by SKN-1/Nrf and the p38 MAPK signaling pathway in Caenorhabditis elegans.
Environ Pollut. 2020 Jan; 256:113382.EP

Abstract

The widespread use of zinc oxide nanoparticles (ZnO-NPs) has led to their release into the environment, and they thus represent a potential risk for both humans and ecosystems. However, the negative impact of ZnO-NPs on the immune system, especially in relation to host defense against pathogenic infection and its underlying regulatory mechanisms, remains largely unexplored. This study investigated the effects of early-life long-term ZnO-NPs exposure (from L1 larvae to adults) on innate immunity and its underlying mechanisms using a host-pathogen Caenorhabditis elegans model, and this was compared with the effect of ionic Zn. The results showed that the ZnO-NPs taken up by C. elegans primarily accumulated in the intestine and that early-life long-term ZnO-NPs exposure at environmentally relevant concentrations (50 and 500 μg/L) decreased the survival of wild-type C. elegans when faced with pathogenic Pseudomonas aeruginosa PA14 infection. Early-life long-term ZnO-NPs (500 μg/L) exposure significantly increased (by about 3-fold) the accumulation of live P. aeruginosa PA14 colonies in the intestine of C. elegans. In addition, ZnO-NPs (500 μg/L) inhibited the intestinal nuclear translocation of SKN-1 and also downregulated gcs-1 gene expression, which is an SKN-1 target gene. Further evidence revealed that early-life long-term exposure to ZnO-NPs (500 μg/L) did not increase susceptibility to mutation among the genes (pmk-1, sek-1, and nsy-1) encoding the p38 mitogen-activated protein kinase (MAPK) cascade in response to P. aeruginosa PA14 infection, though ZnO-NPs significantly decreased the mRNA levels of pmk-1, sek-1, and nsy-1. This study provides regulatory insight based on evidence that ZnO-NPs suppress the innate immunity of C. elegans and highlights the potential health risks of certain environmental nanomaterials, including ZnO-NPs, in terms of their immunotoxicity at environmentally relevant concentrations.

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Publisher Full Text (DOI)

Authors+Show Affiliations

Li SW
Department of Bioenvironmental Systems Engineering, National Taiwan University, Taipei 106, Taiwan.
Huang CW
Department of Bioenvironmental Systems Engineering, National Taiwan University, Taipei 106, Taiwan.
Liao VH
Department of Bioenvironmental Systems Engineering, National Taiwan University, Taipei 106, Taiwan. Electronic address: vivianliao@ntu.edu.tw.

MeSH

AnimalsCaenorhabditis elegansCaenorhabditis elegans ProteinsDNA-Binding ProteinsEcosystemImmunity, InnateMAP Kinase Signaling SystemNanoparticlesPseudomonas aeruginosaTranscription FactorsZinc Oxidep38 Mitogen-Activated Protein Kinases

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31662252

Citation

Li, Shang-Wei, et al. "Early-life Long-term Exposure to ZnO Nanoparticles Suppresses Innate Immunity Regulated By SKN-1/Nrf and the P38 MAPK Signaling Pathway in Caenorhabditis Elegans." Environmental Pollution (Barking, Essex : 1987), vol. 256, 2020, p. 113382.
Li SW, Huang CW, Liao VH. Early-life long-term exposure to ZnO nanoparticles suppresses innate immunity regulated by SKN-1/Nrf and the p38 MAPK signaling pathway in Caenorhabditis elegans. Environ Pollut. 2020;256:113382.
Li, S. W., Huang, C. W., & Liao, V. H. (2020). Early-life long-term exposure to ZnO nanoparticles suppresses innate immunity regulated by SKN-1/Nrf and the p38 MAPK signaling pathway in Caenorhabditis elegans. Environmental Pollution (Barking, Essex : 1987), 256, 113382. https://doi.org/10.1016/j.envpol.2019.113382
Li SW, Huang CW, Liao VH. Early-life Long-term Exposure to ZnO Nanoparticles Suppresses Innate Immunity Regulated By SKN-1/Nrf and the P38 MAPK Signaling Pathway in Caenorhabditis Elegans. Environ Pollut. 2020;256:113382. PubMed PMID: 31662252.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Early-life long-term exposure to ZnO nanoparticles suppresses innate immunity regulated by SKN-1/Nrf and the p38 MAPK signaling pathway in Caenorhabditis elegans. AU - Li,Shang-Wei, AU - Huang,Chi-Wei, AU - Liao,Vivian Hsiu-Chuan, Y1 - 2019/10/16/ PY - 2019/07/09/received PY - 2019/09/26/revised PY - 2019/10/11/accepted PY - 2019/10/31/pubmed PY - 2020/2/25/medline PY - 2019/10/31/entrez KW - Caenorhabditis elegans KW - Early-life long-term exposure KW - Innate immunity KW - SKN-1 KW - Zinc oxide nanoparticles (ZnO-NPs) KW - p38 MAPK pathway SP - 113382 EP - 113382 JF - Environmental pollution (Barking, Essex : 1987) JO - Environ Pollut VL - 256 N2 - The widespread use of zinc oxide nanoparticles (ZnO-NPs) has led to their release into the environment, and they thus represent a potential risk for both humans and ecosystems. However, the negative impact of ZnO-NPs on the immune system, especially in relation to host defense against pathogenic infection and its underlying regulatory mechanisms, remains largely unexplored. This study investigated the effects of early-life long-term ZnO-NPs exposure (from L1 larvae to adults) on innate immunity and its underlying mechanisms using a host-pathogen Caenorhabditis elegans model, and this was compared with the effect of ionic Zn. The results showed that the ZnO-NPs taken up by C. elegans primarily accumulated in the intestine and that early-life long-term ZnO-NPs exposure at environmentally relevant concentrations (50 and 500 μg/L) decreased the survival of wild-type C. elegans when faced with pathogenic Pseudomonas aeruginosa PA14 infection. Early-life long-term ZnO-NPs (500 μg/L) exposure significantly increased (by about 3-fold) the accumulation of live P. aeruginosa PA14 colonies in the intestine of C. elegans. In addition, ZnO-NPs (500 μg/L) inhibited the intestinal nuclear translocation of SKN-1 and also downregulated gcs-1 gene expression, which is an SKN-1 target gene. Further evidence revealed that early-life long-term exposure to ZnO-NPs (500 μg/L) did not increase susceptibility to mutation among the genes (pmk-1, sek-1, and nsy-1) encoding the p38 mitogen-activated protein kinase (MAPK) cascade in response to P. aeruginosa PA14 infection, though ZnO-NPs significantly decreased the mRNA levels of pmk-1, sek-1, and nsy-1. This study provides regulatory insight based on evidence that ZnO-NPs suppress the innate immunity of C. elegans and highlights the potential health risks of certain environmental nanomaterials, including ZnO-NPs, in terms of their immunotoxicity at environmentally relevant concentrations. SN - 1873-6424 UR - https://www.unboundmedicine.com/medline/citation/31662252/Early_life_long_term_exposure_to_ZnO_nanoparticles_suppresses_innate_immunity_regulated_by_SKN_1/Nrf_and_the_p38_MAPK_signaling_pathway_in_Caenorhabditis_elegans_ DB - PRIME DP - Unbound Medicine ER -