Silver nanoparticles induce oocyte maturation in zebrafish (Danio rerio)

Abstract

Public concern regarding silver nanoparticles (AgNPs) in the environment has been increasing since they can cause adverse effects in some aquatic species. However, few data are actually available on the effects of AgNPs on the germ cells. In the present study, we used the zebrafish ovarian follicle as a model to assess the potentially adverse effects of AgNPs on oocyte maturation (germinal vesicle breakdown, GVBD) in vitro. Similar to the maturation inducing hormone (17α, 20β-dihydroxy-4-pregnen-3-one), AgNPs induced GVBD, and reduced the total cyclic adenosine monophosphate (cAMP) concentration in zebrafish ovarian follicles. The results from transmission electron microscope observation and Hoechst 33342 staining clearly indicated that AgNPs induced apoptosis in ovarian follicle cells surrounding the oocyte. Similar to AgNPs, AgNO3 also induced GVBD, decreased cAMP concentration and induced apoptosis of ovarian follicle cells. However, the results from gene expression analysis showed that transcript levels of oxidative stress related genes were more sensitive to AgNPs than AgNO3. Further more, H2O2 has an ability to induce zebrafish oocytes maturation by induction of apoptosis in ovarian follicle cells. Taken together, the results from our study indicated that oxidative stress appeared to be one of important mechanisms in AgNP induced apoptosis in ovarian follicle cells, which further triggered the GVBD.

Zebrafish as a Model to Evaluate Nanoparticle Toxicity

“…The high fecundity rates of zebrafish are well suited to assessing the impact of agents on various aspects of reproduction, from egg production to fertilization rates to subsequent embryo viability. For example, reduced egg production and increased embryo mortality represent a hallmark of chronic exposure with TiO 2 NPs [ 37 ], while in contrast Ag NPs mediated enhanced maturation of zebrafish oocytes due to increased oxidative stress and resultant follicle cell apoptosis [ 38 ].…”

“…Zebrafish have been utilized for a myriad of nanotoxicology studies [ 36 , 37 , 38 , 48 , 70 , 71 ]. A summary of key studies involving the analysis of metal, metal oxide and carbon-based nanoparticles, particularly those related to shape, size and surface charge are discussed below, with relative toxicity summarized ( Table 1 ).…”

Nanoparticles and female reproductive system: how do nanoparticles affect oogenesis and embryonic development

“…Additionally, studies provided evidence that the toxicity to oocytes increased with the silver molar fraction [ 31 - 33 ]. An in vitro model of zebrafish ovarian follicle cells surrounding an oocyte, thecal cells and granulosa cells exhibited apoptosis with phenotypes of irregular cell morphology, disorganized cytoplasm and fragmented and condensed nuclei after exposure to Ag NPs (30 mg/mL) and AgNO 3 (10 mg/mL) [ 34 ]. In vitro experiments also showed that quantum dot-transferrin (QD-Tf) bioconjugates were mostly taken up by the cumulus cells, but no QDs entered the oocytes.…”

Ultrastructural evaluation of oocyte envelopes of zebrafish (Danio Rerio) (Hamilton, 1822) after TiO2 nanoparticle exposure

“…Histologic examinations revealed that empty follicular structures were formed within the ovary tissue. Chen et al [25] reported that silver nanoparticles (used in biosensors, chemical sensors, cosmetics industry, medicine and the paint industry) induce oocyte maturation in zebrafish, promote apoptosis in follicular cells surrounding the oocyte, induce germinal vesicle breakdown, decrease cAMP concentration and cause apoptosis of ovarian follicle cells. Paraptosis has been characterized by chromatin condensation, cytoplasmic vacuolization with many small vacuoles created in the cytoplasm, the widening of the perinuclear space, mitochondrial vesiculation and mitochondrial swelling [26,27].…”