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Impact of Graphene Oxide on Human Placental Trophoblast Viability, © 2018 IOP Publishing Ltd RECEIVED Functionality and Barrier Integrity 11 December 2017 2D MATER

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Impact of Graphene Oxide on Human Placental Trophoblast Viability, © 2018 IOP Publishing Ltd RECEIVED Functionality and Barrier Integrity 11 December 2017 2D MATER IOP 2D Materials 2D Mater. 5 (2018) 035014 https://doi.org/10.1088/2053-1583/aab9e2 2D Mater. 5 OPEN ACCESS PAPER 2018 Impact of graphene oxide on human placental trophoblast viability, © 2018 IOP Publishing Ltd RECEIVED functionality and barrier integrity 11 December 2017 2D MATER. REVISED Melanie Kucki1,4 , Leonie Aengenheister1,4 , Liliane Diener1, Alexandra V Rippl1, Sandra Vranic2 , 8 March 2018 Leon Newman2 , Ester Vazquez3 , Kostas Kostarelos2 , Peter Wick1 and Tina Buerki-Thurnherr1 ACCEPTED FOR PUBLICATION 1 035014 27 March 2018 Laboratory for Particles-Biology Interactions, Empa—Swiss Federal Laboratories for Materials Science and Technology, Lerchenfeldstrasse 5, CH-9014 St. Gallen, Switzerland PUBLISHED 2 27 April 2018 Nanomedicine Laboratory, Faculty of Medical & Human Sciences and National Graphene Institute, University of Manchester, M13 9PT, M Kucki et al Manchester, United Kingdom 3 Departamento de Química Orgánica, Facultad de Ciencias y Tecnologías Químicas-IRICA, Universidad de Castilla-LaMancha, Original content from Av. Camilo Jose Cela, 10 13071 Ciudad Real, Spain this work may be used — 4 under the terms of the Contributed equally to this paper. Creative Commons E-mail: [email protected], [email protected], [email protected], [email protected], Attribution 3.0 licence. [email protected], [email protected], [email protected], [email protected], Any further distribution [email protected] and [email protected] of this work must maintain attribution Keywords: graphene oxide, placenta barrier, nanosafety, barrier integrity to the author(s) and the title of the work, journal Supplementary material for this article is available online 2DM citation and DOI. 10.1088/2053-1583/aab9e2 Abstract Graphene oxide (GO) is considered a promising 2D material for biomedical applications. However, 3 the biological health effects of GO are not yet fully understood, in particular for highly sensitive populations such as pregnant women and their unborn children. Especially the potential impact of GO on the human placenta, a transient and multifunctional organ that enables successful pregnancy, 2053-1583 has not been investigated yet. Here we performed a mechanistic in vitro study on the placental uptake and biological effects of four non-labelled GO with varying physicochemical properties using the 1 human trophoblast cell line BeWo. No overt cytotoxicity was observed for all GO materials after 48 h of exposure at concentrations up to 40 µg ml−1. However, exposure to GO materials induced a slight decrease in mitochondrial activity and human choriogonadotropin secretion. In addition, GO 15 induced a transient opening of the trophoblast barrier as evidenced by a temporary increase in the translocation of sodium fuorescein, a marker molecule for passive transport. Evidence for cellular uptake of GO was found by transmission electron microscopy analysis, revealing uptake of even large micro-sized GO by BeWo cells. Although GO did not elicit major acute adverse effects on BeWo trophoblast cells, the pronounced cellular internalization as well as the potential adverse effects on hormone release and barrier integrity warrants further studies on the long-term consequences of GO on placental functionality in order to understand potential embryo-fetotoxic risks. Introduction shown that several NPs can cross the placental barrier in dependence of the particle properties (e.g. Nanomaterials have attracted great attention as size) and surface modifcations but the underlying candidates for nanomedical applications, e.g. as transfer mechanisms are only poorly investigated and contrast agents and drug nanocarriers [1]. Targeted understood [2, 3]. But even in the absence of placental drug delivery using nanoparticles (NPs) offers the translocation NPs may induce placental damage, possibility to deliver drugs to specifc cells and tissues thereby causing potential indirect embryo-fetotoxicity which increases effcacy and enables to minimize [4–8]. undesired side effects of the drug. Nevertheless, Graphene-related materials (GRM) and other 2D concerns have been raised regarding potential adverse materials have recently attracted a lot of interest in effects of NPs entering the blood stream, especially respect to nano- and biomedical application [9–18]. 30 for sensitive populations including pregnant women Especially water dispersible graphene oxide (GO) is and developing fetus. In the recent years it has been under investigation as potential drug delivery platform April © 2018 IOP Publishing Ltd 2018 2D Mater. 5 (2018) 035014 M Kucki et al [19]. Due to the sheet character of 2D materials GO migration of fetal capillaries closer to the basal lamina exhibits a large surface area for attachment of target- [2, 31, 32]. ing ligands and allows facile functionalization. Never- The aim of the here presented study was to explore theless, effects of GO exposure need to be understood the potential infuence of label-free GO materials with before considering its biomedical application. While distinct physicochemical properties on viability and some in vitro studies report negative acute effects on function of human trophoblasts, which constitutes the exposed cells, others found no cytotoxicity [20–22], as frst and rate-limiting cell layer of the placental barrier. reviewed by Kiew et al [23]. A recent study in mice has For this purpose we applied a well-established 2D cell demonstrated rapid clearance of GO from the blood culture model, namely the human choriocarcinoma stream after intravenous application [10]. Neverthe- cell line BeWo (b30 clone). The BeWo cell line exhibits less, GO has the potential to reach the placenta in sig- several characteristics of human trophoblasts in vivo nifcant amounts as this is a highly perfused organ that including the production of placental hormones such is extensively exposed to circulating substances. as human choriogonadotropin (hCG) [33–35], and To date the impact of 2D-materials on the human the b30 clone can form a tight monolayer if cultivated placental barrier has not been investigated yet (in vitro, on a microporous membrane [36, 37]. Acute toxicity in vivo, ex vivo). However, a profound knowledge on studies were performed including impact of GO on cell the impact of GO at the placental barrier is required viability, barrier integrity, hormone production and for the safe design of GO materials for medical or con- cellular uptake. Only non-labelled GO samples were sumer applications in pregnancy. For other members applied to prevent any artefacts derived from func- of the carbon family such as single-walled and multi- tionalization with linkers and labelling agents which walled carbon nanotubes, indirect and direct feto- bear the potential to alter cellular uptake behaviour. toxic effects were found in animal studies [5, 24–26]. Xu et al investigated the potential impact of rGO on Materials and methods mice and pregnancy after injection of rGO via the tail vein. Female mice exposed to rGO before pregnancy Graphene-related materials (GRM) and or in early gestational stage (~6 d) gave birth to mostly physicochemical characterization healthy offspring, but some malformed mouse fetuses Graphene oxide 1 (GO1) was obtained from Cheap were observed after injection of rGO at early gesta- Tubes (Battleboro, 112 Mercury Drive, VT05301, USA; tional phase. Furthermore, injection of rGO in late www.cheaptubes.com). GO4 was provided by Grupo gestational phase (~20 d) led to abortions as well as Antolin, Spain. GO1 and GO4 were characterized as death of the mothers dependent on the applied rGO described in Kucki et al [21]. concentration [27]. Xu et al assumed that there was no Graphite fakes (Grafake 9580) were obtained transfer of small rGO from the circulation of the dam from Nacional Grafte Ltd (Brazil) and used for the to the fetus, but that a negative effect on the mother’s preparation of large and small graphene oxide (l-GO health resulted in indirect fetotoxic effects [27]. These (f3) and s-GO (f3)). Graphene oxide sheets were studies indicate that GRM bear the potential to exhibit synthesized using the modifed Hummers method negative (direct or indirect) effects on pregnancy, previously described [38, 39]. Briefy, 0.8 g of graph- placental homeostasis and function, as well as on the ite fakes was mixed with 0.4 g of sodium nitrate in a developing fetus. round-bottom fask, and then 18.4 ml of sulfuric acid Nevertheless, it should be noted that the results 99.999% was added slowly to the mixture. After a from animal studies cannot be directly extrapolated homogenized mixture was obtained, 2.4 g of potassium to humans as the placenta is the most species-specifc permanganate was slowly added and the mixture was organ with unique structure and function [28–30]. maintained for 30 min. Next, 37 ml of water for injec- In brief, the human placenta develops during preg- tion was added dropwise due to the violent exothermic nancy in order to meet the changing needs of the grow- reaction, and the temperature was continuously moni- ing fetus. The placental barrier separating the maternal tored and kept at 98 °C for 30 min. The mixture was and fetal blood stream is composed of four layers when further diluted with 112 ml of water for injection, and matured: a multinucleated, single layered syncytio- 30% hydrogen peroxide was added for the reduction trophoblast (ST), a mononucleated but multilayered of the residual potassium permanganate, manganese cytotrophoblast (CT), and the fetal stroma containing dioxide, and manganese heptoxide to soluble manga- fbroblasts, macrophages and the endothelial cells of nese sulfate salts. The resulting mixture was purifed the fetal capillaries. While the ST is non-proliferative, by several centrifugation steps at 9000 rpm for 20 min the CT cells propagate and replenish the ST layer. As until a viscous orange/brown layer of pure GO started pregnancy progresses, the materno-fetal exchange is to appear on top of the oxidation by-products at neu- enhanced due to a signifcant reduction of the placen- tral pH.
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