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Molecular characterization and toxicological effects of citrate-coated silver nanoparticles in a terrestrial invertebrate, the earthworm (Eisenia fetida)

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Abstract

Silver is one of the most popular metals for use in synthesizing metal-based nanoparticles. Silver nanoparticles (AgNPs) are intensively applied within many industrial sectors. Previously, we observed unusual avoidance behavior in earthworms (Eisenia fetida) exposed to AgNPs. To understand the molecular basis of this abnormality, earthworms were exposed to AgNPs (1, 10, 100 mg/kg) or AgNO3 (100 mg/kg, positive control) via the soil to evaluate reactive oxygen species generation, genotoxicity, and transcriptional levels of stress-related genes (catalase, glutathione-Stransferase, heat shock protein 70, metallothionein, and superoxide dismutase). Earthworms exhibited a low propensity to accumulate silver, indicating a reduced mobility of AgNPs in the soil environment. Although abnormal behaviors were not found at low AgNPs concentrations, oxidative stress-related indicators were present, illustrating the importance of molecular responses as sensitive initial biomarkers of AgNP terrestrial contamination. The current study suggests that AgNPs may regulate oxidative stress-related mechanisms and provides an improved understanding of the environmental health effects of AgNPs on species in soil ecosystems.

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References

  1. Schlich, K., Klawonn, T., Terytze, K. & Hund-Rinke, K. Effects of silver nanoparticles and silver nitrate in the earworm reproduction test. Environ Toxicol Chem 32:181–188 (2013).

    Article  PubMed  CAS  Google Scholar 

  2. Mueller, N. C. & Nowack, B. Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453 (2008).

    Article  PubMed  CAS  Google Scholar 

  3. Tourinho, P. S. et al. Metal-based nanoparticles in soil: fate behavior, and effects on soil invertebrates. Environ Toxicol Chem 31:1679–1692 (2012).

    Article  PubMed  CAS  Google Scholar 

  4. Sagee, O., Dror, I. & Berkowitz, B. Transport of silver nanoparticles (AgNPs) in soil. Chemosphere 88:670–675 (2012).

    Article  PubMed  CAS  Google Scholar 

  5. Spurgeon, D. J. et al. Review of subtethalecotoxicological tests for measuring harm in terrestrial ecosystems. Technical Report P5-063/TR1, Environment Agency, Bristol, UK. (2002)

  6. Klobucar, G. et al. Aporrectodea caliginosa, a suitable earthworm species for field based genotoxicity assessment? Environ Pollut 159:841–849 (2011).

    Article  PubMed  CAS  Google Scholar 

  7. Roh, J. Y. et al. Ecotoxicity of silver nanoparticles on the soil nematode Caenorhabditis elegans using functional ecotoxicogenomics. Environ Sci Technol 43:3933–3940 (2009).

    Article  PubMed  CAS  Google Scholar 

  8. Lim, D. et al. Oxidative stress-related PMK-1 P38 MAPK activation as a mechanism for toxicity of silver nanoparticles to reproduction in the nematode Caenorhabditis elegans. Environ Toxicol Chem 31:585–592 (2012).

    Article  PubMed  CAS  Google Scholar 

  9. Shoults-Wilson, W. A. et al. Effect of silver nanoparticle surface coating on bioaccumulation and reproductive toxicity in earthworms (Eisenia fetida). Nanotoxicology 5:432–444 (2011).

    Article  PubMed  CAS  Google Scholar 

  10. Heckmann, L. H. et al. Limit-test toxicity screening of selected inorganic nanoparticles to the earthworm Eisenia fetida. Ecotoxicology 20:226–233 (2011).

    Article  PubMed  CAS  Google Scholar 

  11. Shoults-Wilson, W. A. et al. Evidence for avoidance of Ag nanoparticles by earthworms (Eisenia fetida). Ecotoxicology 20:385–396 (2011).

    Article  PubMed  CAS  Google Scholar 

  12. Tsyusko, O. V. et al. Short-term molecular-level effects of silver nanoparticle exposure on the earthworm, Eisenia fetida. Environ Pollut 171:249–255 (2012).

    Article  PubMed  CAS  Google Scholar 

  13. Lapied, E., Moudilou, E., Exbrayat, J. M., Oughton, D. H. & Joner, E. J. Silver nanoparticle exposure causes apoptotic response in the earthworm Lumbricus terrestris (Oligochaeta). Nanomedicine 5:975–984 (2010).

    Article  PubMed  CAS  Google Scholar 

  14. Asare, N. et al. Cytotoxic and genotoxic effects of silver nanaoparticles in testicular cells. Toxicology 291: 65–72 (2012).

    Article  PubMed  CAS  Google Scholar 

  15. Nymark, P. et al. Genotoxicity of polyvinylpyrrolidonecoated silver nanoparticles in BEAS 2B cells. Toxicology 313:38–48 (2013).

    Article  PubMed  CAS  Google Scholar 

  16. Hayashi, Y. et al. Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticls. Environ Sci Technol 46:4166–4173 (2012).

    Article  PubMed  CAS  Google Scholar 

  17. Coutris, C., Hertel-Aas, T., Lapied, E., Joner, E. J. & Oughton, D. H. Bioavailability of cobalt and silver nanoparticle to the earthworm Eisenia fetida. Nanotoxicology 6:186–195 (2012).

    Article  PubMed  CAS  Google Scholar 

  18. Fabrega, J., Luoma, S. N., Tyler, C. R., Galloway, T. S. & Lead, J. R. Silver nanoparticles: Behaviour and effects in the aquatic environment. Environ Int 37:517–531 (2011).

    Article  PubMed  CAS  Google Scholar 

  19. Cornelis, G. et al. Retention and dissolution of engineered silver nanoparticles in natural soils. Soil Sci Soc Am J 76:891–902 (2012).

    Article  CAS  Google Scholar 

  20. Darlington, T. K., Neigh, A. M., Spencer, M. T., Nguyen, O. T. & Oldenburg, S. J. Nanoparticle characteristics affecting environmental fate and transport through soil. Environ Toxicol Chem 28:1191–1199 (2009).

    Article  PubMed  CAS  Google Scholar 

  21. Unrine, J. M. et al. Evidence for bioavailability of Au nanoparticles from soil and biodistribution within earthworms (Eisenia fetida). Environ Sci Technol 44: 8308–8313 (2010).

    Article  PubMed  CAS  Google Scholar 

  22. Nair, P. M. G., Park, S. Y., Lee, S. & Choi, J. Differential expression of ribosomal protein gene, gonadotrophin releasing hormone gene and Balbiani ring protein gene in silver nanoparticles exposed Chironomus riparius. Aquatic Toxicol 101:31–37 (2011).

    Article  CAS  Google Scholar 

  23. Vijayavel, K. & Balasubramanian, M. P. DNA damage and cell necrosis induced by naphthalene due to the modulation of biotransformation enzymes in an estuarine crab Scylla serrate. J Biochem Mol Toxicol 22:1–7 (2008).

    Article  PubMed  CAS  Google Scholar 

  24. Tomasello, B. et al. Biochemical and bioaccumulation approaches for investigating marine pollution using Mediterranean rainbow wrasse, Coris julis (Linneaus 1798). Ecotoxicol Environ Saf 86:168–175 (2012).

    Article  PubMed  CAS  Google Scholar 

  25. Long, T. C. et al. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect 115:1631–1637 (2007).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  26. Lin, D., Zhou, Q., Xu, Y., Chen, C. & Li, Y. Physiological and molecular responses of the earthworm (Eisenia fetida) to soil chlortetracycline contamination. Environ Pollut 171:46–51 (2012).

    Article  PubMed  CAS  Google Scholar 

  27. Rinna, A. et al. Effect of silver nanoparticles on mitogen-activated protein kinases activation: role of reactive oxygen species and implication in DNA damage. Mutagenesis 30:59–66 (2015).

    Article  PubMed  CAS  Google Scholar 

  28. Bigorgne, E. et al. Ecotoxicological assessment of TiO2 byproducts on the earthworm Eisenia fetida. Environ Pollut 159:2698–2705 (2011).

    Article  PubMed  CAS  Google Scholar 

  29. Lee, K. W. et al. Expression of glustathione S. transferase (GST) genes in marine copepod Tigriopus japonicas exposed to trace metals. Aquat Toxicol 89:158–166 (2008).

    Article  PubMed  CAS  Google Scholar 

  30. Nair, P. M. G., Park, S. Y. & Choi, J. Evaluation of the effect of silver nanoparticles and silver ions using stress responsive gene expression in Chironomus riparius. Chemosphere 92:592–599 (2013).

    Article  PubMed  CAS  Google Scholar 

  31. Hayashi, Y., Heckmann, L. H., Simonsen, V. & Scott-Fordsmand, J. J. Time-course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia fetida. Ecotoxicol Environ Saf 98:219–226 (2013).

    Article  PubMed  CAS  Google Scholar 

  32. Gomes, S. I., Soares, A. M., Scott-Fordsmand, J. J. & Amorim, M. J. Mechanisms of response to silver nanoparticles on Enchytraeus albidus (Oligochaeta): survival, reproduction and gene expression profile. J Hazard Mater 254-255:336–344 (2013).

    Article  PubMed  CAS  Google Scholar 

  33. Hou, W. C., Westerhoff, P. & Posner, J. D. Biological accumulation of engineered nanomaterials: a review of current knowledge. Environ Sci 15:103–122 (2013).

    CAS  Google Scholar 

  34. OECD Guideline for Testing of Chemicals. No. 207. Earthworm Acute Toxicity Test. Organisation for Economic Cooperation and Development, Paris 1984. wwwoecd-ilibraryorg/OECD207pdf (1984).

  35. Eyambe, G. S., Goven, A. J., Fitzpatrick, L. C., Venables, B. J. & Cooper, E. L. A non-invasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Lab Anim 25:61–67 (1991).

    Article  PubMed  CAS  Google Scholar 

  36. Diogene, J., Dufour, M., Poirier, G. G. & Nadeau, D. Extrusion of earthworm coelomocytes: comparison of the cell populations recovered from the species Lumbricus terrestris, Eisenia fetida and Octolasiontyrtaeum. Lab Anim 31:326–336 (1997).

    Article  PubMed  CAS  Google Scholar 

  37. Olive, P. L., Wlodek, D. & Banath, J. P. DNA doublestrand breaks measured in individual cells subjected to gel electrophoresis. Cancer Res 51:4671–4676 (1991).

    PubMed  CAS  Google Scholar 

  38. Barja, G. The quantitative measurement of H2O2 generation in isolated mitochondria. J Bioenerg Biomem 34:227–233 (2002).

    Article  CAS  Google Scholar 

  39. Julian, D., April, K. L., Patel, S., Stein, J. R. & Wohlgemuth, S. E. Mitochondrial depolarization following hydrogen sulfide exposure in erythrocytes from a sulfide-tolerant marine invertebrate. J Exp Biol 208:4109–4122 (2005).

    Article  PubMed  CAS  Google Scholar 

  40. Chen, C., Zhou, Q., Liu, S. & Xiu, Z. Acute toxicity, biochemical and gene expression responses of the earthworm Eisenia fetida exposed to polycyclic musks. Chemosphere 83:1147–1154 (2011).

    Article  PubMed  CAS  Google Scholar 

  41. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real time quantitative PCR and the 2-ΔΔCt method. Methods 25:402–408 (2001).

    Article  PubMed  CAS  Google Scholar 

  42. Park, J. W., Heah, T. P., Gouffon, J. S., Henry, T. B. & Sayler, G. S. Global gene expression in larval zebrafish (Danio rerio) exposed to selective serotonin reuptake inhibitors (fluoxetine and sertraline) reveals unique expression profiles and potential biomarkers of exposure. Environ Pollut 167:163–170 (2012).

    Article  PubMed  CAS  Google Scholar 

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Correspondence to June-Woo Park.

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Choi, J.S., Park, JW. Molecular characterization and toxicological effects of citrate-coated silver nanoparticles in a terrestrial invertebrate, the earthworm (Eisenia fetida). Mol. Cell. Toxicol. 11, 423–431 (2015). https://doi.org/10.1007/s13273-015-0045-z

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  • DOI: https://doi.org/10.1007/s13273-015-0045-z

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