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A Multiparametric Study of Internalization of Fullerenol C60(OH)

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International Journal of Molecular Sciences Article A Multiparametric Study of Internalization of Fullerenol C60(OH)36 Nanoparticles into Peripheral Blood Mononuclear Cells: Cytotoxicity in Oxidative Stress Induced by Ionizing Radiation Anna Lichota 1, Ireneusz Piwo ´nski 2 , Sylwia Michlewska 3,4 and Anita Krokosz 5,* 1 Department of Molecular Biophysics, Faculty of Biology and Environmental Protection, University of Lodz, 90-236 Lodz, Poland 2 Department of Materials Technology and Chemistry, Faculty of Chemistry, University of Lodz, 90-236 Lodz, Poland 3 Laboratory of Electron Microscopy, Faculty of Biology and Environmental Protection, University of Lodz, 90-236 Lodz, Poland 4 Department of General Biophysics, Faculty of Biology and Environmental Protection, University of Lodz, 90-236 Lodz, Poland 5 Department of Biophysics of Environmental Pollution, Faculty of Biology and Environmental Protection, University of Lodz, 90-236 Lodz, Poland * Correspondence: [email protected]; Tel.: +48-42-635-4475 Received: 29 February 2020; Accepted: 24 March 2020; Published: 26 March 2020 Abstract: The aim of this study was to investigate the uptake and accumulation of fullerenol C60(OH)36 into peripheral blood mononuclear cells (PBMCs). Some additional studies were also performed: measurement of fullerenol nanoparticle size, zeta potential, and the influence of fullerenol on the ionizing radiation-induced damage to PMBCs. Fullerenol C60(OH)36 demonstrated an ability to accumulate in PBMCs. The accumulation of fullerenol in those cells did not have a significant effect on cell survival, nor on the distribution of phosphatidylserine in the plasma membrane. However, fullerenol-induced depolarization of the mitochondrial membrane proportional to the compound level in the medium was observed. Results also indicated that increased fullerenol level in the medium was associated with its enhanced transport into cells, corresponding to its influence on the mitochondrial membrane. The obtained results clearly showed the ability of C60(OH)36 to enter cells and its effect on PBMC mitochondrial membrane potential. However, we did not observe radioprotective properties of fullerenol under the conditions used in our study. Keywords: fullerenol uptake; accumulation; ionizing radiation; mitochondrial membrane potential 1. Introduction Nanomaterials (NMs) are structure components with at least one dimension less than 100 nm. NMs should possess superior properties with enhanced performance that typical materials do not have [1]. Nanoparticles (NPs) are created due to van der Waals forces, electrostatic interactions, hydrogen bonds, as well as capillary bridges. The ability of NPs to assemble and interconnect strongly depends on their physical and chemical characteristics and their surface properties, including size, shape, ratio of electric charges and hydrophobicity, and last, but not least, on the concentration and the presence of functional groups [2,3]. These factors, as well as ability to interact with superficial cellular receptors also determine the rate and mechanism of entry of NMs into a cell [4]. 2.5 Fullerene C60 is a nanomaterial consisting of 60 carbon atoms connected by sp -bonds. Due to those bonds, it has a pseudo-aromatic structure resulting from delocalization of π-electrons over Int. J. Mol. Sci. 2020, 21, 2281; doi:10.3390/ijms21072281 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 20 Int. J. Mol. Sci. 2020, 21, 2281 2 of 18 carbon core. This structure allows easy reaction with oxygen free radicals [4–6]. It was shown that pristinethe carbon C60 core.fullerene This was structure non-toxic allows at easylow concentrations, reaction with oxygen and it free was radicals able to [ 4penetrate–6]. It was cellular shown plasmathat pristine membrane. C60 fullerene It has also was been non-toxic shown at to low exhibi concentrations,t antioxidantand properties it was able[7]. Fullerene to penetrate increases cellular theplasma activity membrane. of antioxidant It has also enzymes been shown and prevents to exhibit de antioxidantleterious effects properties of oxidative [7]. Fullerene stress increases by direct the reactiveactivity oxygen of antioxidant species enzymes (ROS) scavenging and prevents [8]. deleterious The C60 fullerene effects of nanoparticle oxidative stress does by not direct exert reactive any genotoxicoxygen species effect on (ROS) human scavenging lymphocytes. [8]. The C60 C reduces60 fullerene the genotoxic nanoparticle effect does of notdoxorubicin exert any (DOX) genotoxic in normaleffect on human human lymphocytes lymphocytes. [9]. C60 Newreduces fullerene the genotoxic derivatives effect ofcan doxorubicin also be used (DOX) for in upconversion normal human luminescencelymphocytes [(UCL)9]. New and fullerene magnetic derivatives resonance can imagin also beg used (MRI). for upconversionThat may be of luminescence great importance (UCL) andin “image-guidedmagnetic resonance therapy” imaging [10]. (MRI). Fullerenes That may may be be of greatintroduced importance anywhere in “image-guided in the body therapy” and they [10 ]. accumulateFullerenes in may specific be introduced organs, such anywhere as the inliver, the kidneys, body and and they the accumulate spleen. Scientists in specific suggested organs, that such fullerenesas the liver, were kidneys, able to andpass the into spleen. the blood Scientists from the suggested gut and thatcould fullerenes be transported were ablewith to blood pass [11,12]. into the Studiesblood fromhave theshown gut andthat couldfullerenes be transported affected the with order blood of membrane [11,12]. Studies lipids have and showninduced that membrane fullerenes damageaffected by the lipid order peroxidation. of membrane It lipidswas demonstrated and inducedmembrane that they accumulated damage by lipid in lysosomes peroxidation. of oyster It was hepatopancreasdemonstrated thatcells. they The accumulated disposition of in carbon lysosomes NPs of in oyster biological hepatopancreas systems is independent cells. The disposition on the site of ofcarbon contact NPs between in biological NPs systemsand an isorganism. independent It is on related the site to of contactthe passage between across NPs cell and anmembrane. organism. FluorescenceIt is related toquenching the passage showed across that cell membrane.C60(OH)18–22 Fluorescenceaccumulated quenchingin outer regions showed of that the C membrane60(OH)18–22 bilayer,accumulated whereas in outerC60 was regions found of in the deeper membrane regions bilayer, of the whereasbilayer [13,14]. C60 was Other found water-soluble in deeper regions fullerene of the derivatives,bilayer [13, 14such]. Other as the water-soluble dicarboxyfullerenes, fullerene derivatives, concentrate such in asmitochondria the dicarboxyfullerenes, or in endosome- concentrate or lysosome-likein mitochondria vesicles or in [15]. endosome- or lysosome-like vesicles [15]. FullerenolsFullerenols are are bioactive bioactive compounds, compounds, polyhydroxyl polyhydroxylatedated water-soluble water-soluble derivatives derivatives of of fullerenes, fullerenes, 60 x a athird third natural natural allotropic allotropic variation variation of carbon [[5,16,17].5,16,17]. TheThe chemicalchemical structurestructure of of fullerenol fullerenol C 60C(OH)(OH)x is ispresented presented in in Figure Figure1 .1. The The solubility solubility ofof fullerenolfullerenol inin waterwater increases with the increasing number number of of hydroxylhydroxyl groups groups [[18].18]. FullerenolsFullerenols and and malonic malonic acid ac fullereneid fullerene species species are two are major two groups major ofgroups functional of functionalfullerene derivativesfullerene derivatives possessing possessing effective protective effective protective antioxidative antioxidative properties bothpropertiesin vitro bothand inin vitro vivo , andand in having vivo, alsoand antitumorhaving also potential antitumor and potential antimetastatic and antimetastatic activity [19–21 ].activity The results [19–21]. of the The study results carried of 60 2 2 60 22 theout study by Yin carried et al. (2009)out by [22 Yin] indicated et al. (2009) that C 60[22](C(COOH) indicated2) 2,Cthat60 (OH)C (C(COOH)22, and Gd@C) , C82(OH)(OH)22, couldand 82 22 2 2 Gd@Cprotect(OH) cells against could H 2Oprotect2-induced cells oxidative against damage, H O -induced stabilized theoxidative mitochondrial damage, membrane stabilized potential, the mitochondrialand reduced intracellularmembrane potential, ROS production. and reduced Due to intracellular their hydrophilic ROS propertiesproduction. and Due the to ability their to hydrophilicscavenge free properties radicals, and fullerenol the ability could to provide scavenge a valuable free radicals, alternative fullerenol to conventional could provide pharmacological a valuable alternativeagents [17 ].to The conventional effect of polyhydroxylated pharmacological fullerenol agents [17]. NPs The on adulteffect male of polyhydroxylated Wistar rats treated fullerenol with DOX NPswas on investigated adult male by Wistar Jacevic rats et al. treated (2017) with [23]. DOX The authors was investigated reported that by fullerenol Jacevic et increased al. (2017) the [23]. survival The authorsrate, body reported and liver that weight, fullerenol as well increased as decreased the survival the level rate, of thiobarbituric body and liver acid weight, reactive as substances well as decreased(TBARS), antioxidativethe level of enzymethiobarbituric activity, acid and
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