Sensory systems and ionocytes are targets for silver nanoparticle effects in fish

Abstract

Some nanoparticles (NPs) may induce adverse health effects in exposed organisms, but to date the evidence for this in wildlife is very limited. Silver nanoparticles (AgNPs) can be toxic to aquatic organisms, including fish, at concentrations relevant for some environmental exposures. We applied whole mount in-situ hybridisation (WISH) in zebrafish embryos and larvae for a suite of genes involved with detoxifying processes and oxidative stress, including metallothionein (mt2), glutathionine S-transferase pi (gstp), glutathionine S-transferase mu (gstm1), haem oxygenase (hmox1) and ferritin heavy chain 1 (fth1) to identify potential target tissues and effect mechanisms of AgNPs compared with a bulk counterpart and ionic silver (AgNO₃). AgNPs caused upregulation in the expression of mt2, gstp and gstm1 and down regulation of expression of both hmox1 and fth1 and there were both life stage and tissue-specific responses. Responding tissues included olfactory bulbs, lateral line neuromasts and ionocytes in the skin with the potential for effects on olfaction, behaviour and maintenance of ion balance. Silver ions induced similar gene responses and affected the same target tissues as AgNPs. AgNPs invoked levels of target gene responses more similar to silver treatments compared to coated AgNPs indicating the responses seen were due to released silver ions. In the Nrf2 zebrafish mutant, expression of mt2 (24 hpf) and gstp (3 dpf) were either non-detectable or were at lower levels compared with wild type zebrafish for exposures to AgNPs, indicating that these gene responses are controlled through the Nrf2-Keap pathway.

Keywords:

• Danio rerio
• Nrf2 pathway
• oxidative stress
• silver nanoparticles
• target tissues

Acknowledgements

The NERC funded Facility Environmental Nanoscience Analysis and Characterisation (FENAC) is acknowledged for their support in characterisation of the silver materials.

Declaration of interest

The author's affiliation is as shown on the cover page and the authors have sole responsibility for the writing and content of the paper. The literature review conducted, the interpretations made and the conclusions drawn are exclusively those of the authors. None of the authors has any actual or potential competing financial interests. This work was funded by the Natural Environmental Research Council NE/L007371/1 and NE/H013172/1) and the European Union 7th Framework programme (Nanomile; Engineered nanoparticles and mechanisms of interactions with living systems and the environment: a universal framework for safe nanotechnology. This work was supported by the Natural Environmental Research Council (NE/G004862/1), EU FP7 project NANOMILE (NMP4-LA-2013-310451; www.nanomile.eu/), the UK Environment Agency, and the University of Exeter on grants to CRT.

Supplementary material available online