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Fate, cytotoxicity and cellular metabolomic impact of ingested nanoscale carbon dots using simulated digestion and a triculture small intestinal epithelial model.

ABSTRACT: Carbon dots (CDs) are a promising material currently being explored in many industrial applications in the biomedical and agri-food areas; however, studies supporting the environmental health risk assessment of CDs are needed. This study focuses on various CD forms including iron (FeCD) and copper (CuCD) doped CDs synthesized using hydrothermal method, their fate in gastrointestinal tract, and their cytotoxicity and potential changes to cellular metabolome in a triculture small intestinal epithelial model. Physicochemical characterization revealed that 75% of Fe in FeCD and 95% of Cu in CuCD were dissolved during digestion. No significant toxic effects were observed for pristine CDs and FeCDs. However, CuCD induced significant dose-dependent toxic effects including decreases in TEER and cell viability, increases in cytotoxicity and ROS production, and alterations in important metabolites, including D-glucose, L-cysteine, uridine, citric acid and multiple fatty acids. These results support the current understanding that pristine CDs are relatively non-toxic and the cytotoxicity is dependent on the doping molecules.

SUBMITTER: Cao X

PROVIDER: S-EPMC8428805 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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Fate, cytotoxicity and cellular metabolomic impact of ingested nanoscale carbon dots using simulated digestion and a triculture small intestinal epithelial model.

Cao Xiaoqiong X Pan Xiaoyong X Couvillion Sneha P SP Zhang Tong T Tamez Carlos C Bramer Lisa M LM White Jason C JC Qian Wei-Jun WJ Thrall Brian D BD Ng Kee Woei KW Hu Xiao X Demokritou Philip P

NanoImpact 20210701

Carbon dots (CDs) are a promising material currently being explored in many industrial applications in the biomedical and agri-food areas; however, studies supporting the environmental health risk assessment of CDs are needed. This study focuses on various CD forms including iron (FeCD) and copper (CuCD) doped CDs synthesized using hydrothermal method, their fate in gastrointestinal tract, and their cytotoxicity and potential changes to cellular metabolome in a triculture small intestinal epithe ...[more]

PMID: 34514184

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Project description:Nanoscale materials derived from natural biopolymers like cellulose and chitosan have many potentially useful agri-food and oral drug delivery applications. Because of their large and potentially bioactive surface areas and other unique physico-chemical properties, it is essential when evaluating their toxicological impact to assess potential effects on the digestion and absorption of co-ingested nutrients. Here, the effects of cellulose nanofibers (CNF), cellulose nanocrystals (CNC), and chitosan nanoparticles (Chnp) on the digestion and absorption of carbohydrates were studied. Starch digestion was assessed by measuring maltose released during simulated digestion of starch solutions. Glucose absorption was assessed by measuring translocation from the resulting digestas across an in vitro transwell tri-culture model of the small intestinal epithelium and calculating the area under the curve increase in absorbed glucose, analogous to the glycemic index. At 1% w/w, CNF and Chnp had small but significant effects (11% decrease and 14% increase, respectively) and CNC had no effect on starch hydrolysis during simulated digestion of a 1% w/w rice starch solution. In addition, at 2% w/w CNC had no effect on amylolysis in 1% solutions of either rice, corn, or wheat starch. Similarly, absorption of glucose from digestas of starch solutions (i.e., from maltose), was unaffected by 1% w/w CNF or CNC, but was slightly increased (10%, p<0.05) by 1% Chnp, possibly due to the slightly higher maltose concentration in the Chnp-containing digestas. In contrast, all of the test materials caused sharp increases (~1.2, 1.5, and 1.6 fold for CNC, CNF, and Chnp, respectively) in absorption of glucose from starch-free digestas spiked with free glucose at a concentration corresponding to complete hydrolysis of 1% w/w starch. The potential for ingested cellulose and chitosan nanomaterials to increase glucose absorption could have important health implications. Further studies are needed to elucidate the mechanisms underlying the observed increases and to evaluate the potential glycemic effects in an intact in vivo system.

Project description:BackgroundEngineered nanomaterials (ENMs) have already made their way into myriad applications and products across multiple industries. However, the potential health risks of exposure to ENMs remain poorly understood. This is particularly true for the emerging class of ENMs know as 2-dimensional nanomaterials (2DNMs), with a thickness of one or a few layers of atoms arranged in a planar structure.MethodsThe present study assesses the biotransformations and in vitro cytotoxicity in the gastrointestinal tract of 11 2DNMs, namely graphene, graphene oxide (GO), partially reduced graphene oxide (prGO), reduced graphene oxide (rGO), hexagonal boron nitride (h-BN), molybdenum disulphide (MoS2), and tungsten disulphide (WS2). The evaluated pristine materials were either readily dispersed in water or dispersed with the use of a surfactant (Na-cholate or PF108). Materials dispersed in a fasting food model (FFM, water) were subjected to simulated 3-phase (oral, gastric, and small intestinal) digestion to replicate the biotransformations that would occur in the GIT after ingestion. A triculture model of small intestinal epithelium was used to assess the effects of the digested products (digestas) on epithelial layer integrity, cytotoxicity, viability, oxidative stress, and initiation of apoptosis.ResultsPhysicochemical characterization of the 2DNMs in FFM dispersions and in small intestinal digestas revealed significant agglomeration by all materials during digestion, most prominently by graphene, which was likely caused by interactions with digestive proteins. Also, MoS2 had dissolved by ~75% by the end of simulated digestion. Other than a low but statistically significant increase in cytotoxicity observed with all inorganic materials and graphene dispersed in PF108, no adverse effects were observed in the exposed tricultures.ConclusionsOur results suggest that occasional ingestion of small quantities of 2DNMs may not be highly cytotoxic in a physiologically relevant in vitro model of the intestinal epithelium. Still, their inflammatory or genotoxic potential after short- or long-term ingestion remains unclear and needs to be studied in future in vitro and in vivo studies. These would include studies of effects on co-ingested nutrient digestion and absorption, which have been documented for numerous ingested ENMs, as well as effects on the gut microbiome, which can have important health implications.

Dataset Information

Fate, cytotoxicity and cellular metabolomic impact of ingested nanoscale carbon dots using simulated digestion and a triculture small intestinal epithelial model.

Publications

Fate, cytotoxicity and cellular metabolomic impact of ingested nanoscale carbon dots using simulated digestion and a triculture small intestinal epithelial model.

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