Our own work investigated the response of porcine cumulus—oocyte complexes to BSA-coated gold, silver and gold—silver alloy nanoparticles in vitro . Beyond the pure AuNP and AgNP the alloy particles were introduced in order to analyse in how far alloy formation alters the toxic potential of the pure metal nanoparticles. The directly adjacent cumulus cells incorporated gold nanoparticles to a substantially lesser degree.
The gold—silver alloy particles displayed toxicity to oocytes depending on the silver molar fraction they contained. Figure 5: Oocyte maturation rates after 46 h of in vitro maturation in the presence of various nanoparticle types or silver nitrate in the maturation medium during the complete in vitro maturation time.
Figure 5: Oocyte maturation rates after 46 h of in vitro maturation in the presence of various nanoparticle t Figure 6: Representative laser scanning microscope images of porcine cumulus—oocyte complexes after 46 h co-incubation during in vitro maturation. Figure 6: Representative laser scanning microscope images of porcine cumulus—oocyte complexes after 46 h co-i Even though there is no further literature which may be directly compared to our findings, with regard to toxicity our results agree with the general conception of cytotoxic effects excercised by gold and silver nanoparticles, which views silver as potentially more aggressive than gold .
The exact mechanisms by which silver nanoparticles inflict their damage is still a matter of debate. Although the toxicity seems to be driven by oxidation and inflammation  , it is unclear whether silver in its nanoparticulate form is responsible for the toxic effects, as some studies claim  , or whether they are solely caused by silver ions dissolving in the course of oxidation of the metal . More recent and so far unpublished data seems to further confirm the hypothesis, that silver nanoparticle toxicity is mainly derived from the silver ions.
In case of in situ bioconjugation silver nanoparticles are synthesized by laser ablation of a solid target in the presence of the biomolecule of choice [52,79]. The ex situ method is an alternative approach where the ablation site is physically separated from bioconjugation . To this end laser ablation is carried out in a flow through reactor, while biomolecules are added at specified time delays. Innate to the in situ bioconjugation method is a distinct size quenching effect .
However, one has to be cautious to contribute the difference in toxic potential solely to the obvious difference in size. There might be other so far undected differences between the particles, which could have caused the described results, especially as silver nanoparticles keep evolving in biological media . Figure 7: A Number weighted size distribution of AgNP in situ red line and ex situ black line conjugated to bovine serum albumin BSA as measured by disc centrifugation.
Figure 7: A Number weighted size distribution of AgNP in situ red line and ex situ black line conjugate This suggests that incorporation of silver into an alloy structure can be used to control the toxicity of silver nanoparticles, which confirms findings observed after exposing bacterial cultures to gold—silver alloy nanoparticles . The reasons for that phenomenon can only be speculated about.
As these proteins define the biological identity of a particle  , they might be responsible for the variations in particle uptake. The described results confirm that in vitro maturation of oocytes represent a very sensitive system for the exploration of nanotoxicology in which even subtle effects can be visualized.
The use of this test system should be increased in the future to gain a better understanding of possible influences of nanoparticle exposure on female reproduction. Within the field of nanoreprotoxicology embryo development is certainly the most intensively investigated area. Among those experiments many have been conducted by using gold and silver nanoparticles.
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The majority of this research focussed on piscine species, especially zebrafish, because such embryos can be obtained easily and in great numbers. In case of the latter it was shown that surface functionalisation had an additional influence on the severity and the characteristica of the observed toxicity [93,94]. Another interesting point raised was the impact of colloidal stability in the final exposure medium on the toxic potential of gold as well as silver nanoparticles showing a decrease in toxicity with increasing agglomeration, i.
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Internalisation of nanoparticles into the embryos in a concentration dependent manner was also a consistent finding [83,90]. Oxidative stress was confirmed as the predominant mechanism responsible for toxic effects of AgNP on piscine embryos . However, the results derived from marine species under conditions specific for external fertilisation and embryo development cannot simply be extrapolated to other species. This becomes apparent when reprotoxicological studies using chicken embryos, which were exposed in ovo to nanoparticles made from gold  , silver  , silver—palladium alloy  and silver—copper alloy  are considered.
While gold nanoparticles remained consistently inert, even after application of silver containing nanoparticles, no abnormal development was observed, except a low-grade inflammation of the embryonic liver after exposure to AgCu alloy nanoparticles. Similar observations were made when administering gold and silver nanoparticles into pregnant mouse and rat dams respectively [44,]. The reason for the apparent discrepancy between piscine and other species concerning the toxicity of silver-containing nanoparticles could be that the amount of nanoparticles which actually reached the embryo was a lot higher in the trials using piscine species.
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In these cases the particles were applied basically directly to the embryos in a environment of comparatively low complexity. Even though the initial doses in the chicken and rodent studies were comparatively high, the nanoparticles were first exposed to the contents of an egg or even to an entire different organism the dam , which probably reduced the nanoparticle load of the embryo tremendously. In rats for instance it has been reported that of the AuNP dose applied to the mother by intravenous injection the foetus would take up approximately 0.
This is supported by a study where murine preimplantation embryos were exposed in vitro, i. Similar to the trials using piscine embryos, the authors found abnormalities during preimplantation development like increased apoptosis at the blastocyst stage in conjuction with a reduced number of pups if nanoparticle exposed blastocysts where transferred to recipient dams. Therefore, when interpreting such data for its predictive value, the assessment of the exposure dose for its closeness to reality is a critical point.
Interestingly, gold nanoparticles did not seem to trigger any toxicity in embryos regardless of dose . In our own study, the effects of gold and silver nanoparticles on murine embryos was investigated . The particles were microinjected into one blastomere of a 2-cell murine embryo, thus ensuring the delivery of small, i. The sister blastomere remained untreated allowing for an internal control. This increases the sensitivity of the test system by also pointing out sublethal effects, like the interference with cell division mechanisms, which has been described as a toxic effect of gold nanoparticles .
The administered dose of nanoparticles was calculated based on the assumption that an embryo would take up approximately 0. Neither the pre-implantation development of the embryos up to blastocyst stage was impaired, nor could a disregulation of various candidate genes for embryo development be found.
Especially with regard to silver nanoparticles, this result might seem surprising at first. However, our results support the findings of the above mentioned in ovo and in vivo studies [44,98,99,]. Our in vitro study used similar dosages as can be expected after in vivo exposure and we also obtained similar results. This further confounds the hypothesis that the effects seen in studies with direct embryonic exposure to silver nanoparticles derive from extremly high dosages of nanoparticles per embryo.
Therefore, to improve the predictive value of future in vitro studies the experimental design should involve the testing of dosages realistic for in vivo exposure scenarios. However, to facilitate this, more biodistribution studies need to be performed, which firstly should also work with dosages and application routes appropriate for the kind of particle tested and secondly actually include reproductive organs as well as embryos into their examinations. Figure 8: Blastocyst development rates after microinjection of nanoparticles into 2-cell-stage murine embryos AuNP-injection, AgNP-injection, sham injection, handling control adapted from .
Figure 8: Blastocyst development rates after microinjection of nanoparticles into 2-cell-stage murine embryos The results described in this review with regard to the reprotoxicology of gold and silver nanoparticles permit the following conclusions: i Exposure of reproduction relevant cells to gold and silver nanoparticles after systemic administration has been proven. However, a considerable uncertainty exists concerning the particles properties once they arrived at their site of action.
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Especially the surface molecules, which likely define the bio-identity of the particles, will probably have changed after biodistribution compared to the pristine particles. Cellular internalisation depends on cell type as well as particle composition. Spermatozoa showed no evidence of particle uptake at all. Oocytes preferentially internalised pure gold nanoparticles, while gold—silver alloy particles as well as pure silver nanoparticles where mainly found in the cumulus cells surrounding the oocytes.
However, even gold nanoparticles were observed to be toxic to spermatozoa in a concentration dependent manner, in case the nanoparticles possess surface properties that allow direct contact with the sperm plasma membrane. Protein coronas seem to inhibit such contact.
A clearly defined toxic threshold is difficult to determine though, as silver nanoparticle toxicity also depends on particle size as well as particle composition. The latter could distinctly been shown by employing gold—silver alloy colloids as model nanoparticles. Spermatozoa have been shown to be considerable more resistant towards silver nanoparticle derived toxicity, which might be explained by the unique metabolism spermatozoa feature compared to other cells. Future research should aim to establish clear specifications which nanoparticle dose can be expected to be toxic under consideration of particle characteristics obtained under relevant biological conditions.
Additionally, nanoparticle toxicity should not only be asssessed considering cell viability but also concerning functional aspects. To this purpose the investigation of nanotoxicology on reproductive cells provides an ideal tool.