Elsevier

Food Chemistry

Volume 293, 30 September 2019, Pages 387-395
Food Chemistry

Carbon quantum dots from roasted Atlantic salmon (Salmo salar L.): Formation, biodistribution and cytotoxicity

https://doi.org/10.1016/j.foodchem.2019.05.017Get rights and content

Highlights

Abstract

The endogenous carbon quantum dots (CQDs) produced during food processing have potential uncertainty to human health. The objective of this study was to investigate the formation, biodistribution and cytotoxicity of CQDs in roasted Atlantic salmon (Salmo salar Linnaeus). The X-ray photoelectron spectroscopy (XPS) analysis showed that the CQDs were mainly composed of carbon, oxygen and nitrogen. The morphology, functional groups and optical properties were highly dependent on the roasting time. In vivo experiments in mice demonstrated that the CQDs distributed in the digestive tract, kidney, liver, and even brain, which indicated that they could cross the blood–brain barrier. The cell imaging results indicated that the CQDs could readily gain access to the normal rat kidney (NRK) cells, and caused autophagosome formation. The proportion of live cells decreased to 34.62% at 6 mg mL−1 of CQDs, and the energy generation route was changed from aerobic to glycolytic metabolism.

Introduction

Atlantic salmon (Salmo salar L.) is an important seafood, not only for its taste and culinary qualities, but also for its health properties, with regard to its minerals, vitamins, high-quality proteins with essential amino acids, astaxanthin and fatty acids such as omega-3 polyunsaturated fatty acids, particularly eicosapentaenoic acid, docosahexaenoic acid (Costa et al., 2015). The roasted Salmo salar L. is a popular seafood due to its delicious taste and uniquearoma flavor (Ovissipour, Rasco, Tang, & Sablani, 2017). The chemical toxins, such as acrylamide and heterocyclic amines formed in the roasted food, have a positive association with an elevated health risk to the consumer (Chen et al., 2013, Lee et al., 2016). In addition, recent works have reported the endogenous carbon nanoparticles produced in roasted foods, such as the amorphous carbon nano-structures in various food caramels (Sk, Jaiswal, Paul, Ghosh, & Chattopadhyay, 2012), and the carbon dots (CDs) generated from overcooked barbecue meat (Wang et al., 2013). Fluorescent nanoparticles were also reported in roasted pike eel (Bi et al., 2017), grilled hamburger (Li et al., 2017), and baked lamb (Wang et al., 2017, Wang et al., 2017). It is noteworthy that carbon per se is not considered as toxic element. However, exposure to carbon nanostructures in roasted food is of particular concern, as they have unique properties that can be associated with toxicity, such as high surface to volume ratio, photocatalytic activity and enhanced permeability (Nel, Ruoslahti, & Meng, 2017). This is hardly mentioned in the literatures, and our knowledge about the endogenous nanoparticles from roasted food is insufficient.

Carbon nanoparticles have been reported to have certain adverse effects on biological systems (Nel et al., 2015). The metabolic stress in human stem cells was reported to be caused by the carbon nanoparticles derived from bakery products (Al-Hadi, Periasamy, Athinarayanan, & Alshatwi, 2016). The carbon quantum dots (CQDs) could induce cell death, apoptosis and autophagy when they were used as photodynamic agents (Markovic et al., 2012). The CQD-induced reactive oxygen species were found to lead to apoptosis, autophagy, and inflammatory response in THP-1 activated macrophages (Qin et al., 2015). Moreover, the CQDs could suppress proinflammatory T-cell responses through the way of autophagy-dependent induction of tolerogenic monocyte-derived dendritic cells. (Tomiä et al., 2017) To date, the presence of CQDs in roasted foods and their biosafety have not been sufficiently investigated. We have no idea how about the formation of Salmo salar L. CQDs during the roasting process, and whether the CQDs are potentially toxic.

In this work, the formation of Salmo salar L. CQDs was reported for various time periods at 200 °C and the CQD morphology, size, nanostructure, optical properties and functional groups were characterized. By taking the CQDs generated at 200 °C for 50 min as an example, in vitro and in vivo biodistribution, and cytotoxicity were studied in the normal rat kidney (NRK) cell lines. Notably, we found that the Salmo salar L. CQDs can be absorbed and cross the blood–brain barrier (BBB) presenting in the brain of mice. Moreover, the cellular toxicity was investigated by analysis of the cell cycle, apoptosis, autophagy and cell respiration. The hazard assessment of the endogenous CQDs produced in roasted Salmo salar L. provided important evidence for their potential adverse effects.

Section snippets

Materials

Atlantic Salmo salar L. fillets were purchased from the local market in Dalian, China. Glucose was purchased from Beijing Soledad Technology Co., Ltd. (Beijing, China). The macroporous resin D101 and high performance liquid chromatography (HPLC) grade methanol were obtained from Sigma-Aldrich Co. LLC (St. Louis, MO, USA). Dulbecco's modified Eagle’s medium (DMEM) and fetal bovine serum (FBS), were purchased from Biological Industries (BioInd; Kibutz Beit Ha’Emek, Israel). Anti-LC3 antibody and

Structural characterization of Salmo salar L. CQDs

The roasted Salmo salar L. is a kind of favourite seafood and the formation and hazardous effects of CQDs may have a great impact on its consumption due to their potential safety concern. In this work, the CQDs were found for the first time in Salmo salar L. roasted at 200 °C for various periods of time (10, 20, 30, 40, 50 and 60 min) and more experimental details can be found in the support information. TEM images (Fig. 1a–f) reveal that the CQDs are well dispersed, with a particle size that

Conclusion

In summary, different roasting time led to production of Salmo salar L. CQDs with different particle size, surface groups, and fluorescence property. The in vitro cell imaging results revealed that the CQDs can enter into the cytoplasmic and nuclear regions of the NRK cells, while in vivo biodistribution revealed that they were absorbed in the small intestine, and present in the mouse brain. The NRK cells treated with 3 mg mL−1 CQDs induced autophagy and autophagosome formation. The CQDs

Declaration of Competing Interest

The authors declare no competing financial interest.

Acknowledgements

This work was financially supported by the National Key R & D Program of China (2017YFD0400103) and the National Natural Science Foundation of China (31872915).

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