Enrichment of the inorganic analogue of martian dust with the novel carbon nanoparticles obtained during combustion of carbohydrates and assesment of its meurotoxicity

1Pozdnyakova, NG, 1Pastukhov, AO, 1Dudarenko, MV, 1Galkin, MO, 1Krisanova, NV, 1Borisova, TA
1Palladin Institute of Biochemistry of National Academy of Sciences of Ukraine, Kyiv, Ukraine
Space Sci.&Technol. 2018, 24 ;(2):60-71
https://doi.org/10.15407/knit2018.02.060
Section: Space Life Sciences
Publication Language: Ukrainian
Abstract: 
Nowadays, analysis of the mechanisms of brain malfunctioning under conditions of long-term manned space missions is a priority research area of international scientific groups and an urgent task of modern space biology. Ignoring the problems of the nervous system functioning can make impossible further long-term interplanetary space missions. One of the possible causes of brain impairment can be an exposure to planetary and interstellar dust, whose composition,  properties,  and the impact on human health, in particular, neurotoxicity, have not been sufficiently investigated. Carbon is widely distributed in the native Martian dust and interstellar space and is a part of meteorites. In this study, the inorganic analog of Martian dust (MD) (JSC, Mars-1A, ORBITEC Orbital Technologies Corporation, Madison, Wisconsin, USA) was enriched in different amounts by carbon nanoparticles (CNP) synthesized by the combustion of carbohydrates. MD enriched with CNP (CNP-MD) depolarizes the plasma membrane of the rat brain nerve terminals as shown by fluorimetry using a rhodamine 6G fluorescent probe.
                 An increase in the content of the carbon component of the CNP-MD is accompanied by an increase in the depolarization of the membrane. CNP-MD significantly reduces the initial rate of accumulation and increases the extracellular level of the neurotransmitters L-[14C] glutamate and [3H]GABA (g-aminobutyric acid) in the nerve terminals. An increase of CNP content in CNP-MD is accompanied by a more significant decrease in the initial rate of neurotransmitter uptake and an increase in their extracellular level. Therefore, the neurotoxic effect of CNP-MD is associated exclusively with the CNP activity but not with the action of its inorganic component. A decrease in the CNP content in CNP-MD reduces its neurotoxicity.
Keywords: brain nerve terminals, L-[14С]glutamate, Martian dust analogue; carbon nanoparticles, membrane potential, synaptosomes, [3Н]GABA
References: 
1. Abbott N. J. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol., 2, 131—147 (2000).
2. Allamandola L. J., Sandford S. A., Wopenka B. Interstellar polycyclic aromatic hydrocarbons and carbon in interplanetary dust particles and meteorites. Science, 4810, 56—9 (1987).
https://doi.org/10.1126/science.237.4810.56
3. Bhunia S. K., Saha A., Maity A. R., et al. Carbon nanoparticle-based fluorescent bioimaging probes. Sci. Rep., 1, 1473 (2013).
4. Borisova T., Dekaliuk M., Pozdnyakova N., et al. Harmful impact on presynaptic glutamate and gaba transport by carbon dots synthesized from sulfur-containing carbohydrate precursor. Environ. Sci. Pollut. Res., 21, 17688— 17700 (2017).
5. Borisova T., Krisanova N., Sivko R., Borysov A. Cholesterol depletion attenuates tonic release but increases the ambient level of glutamate in rat brain synaptosomes. Neurochem. Int., 3, 466—478 (2010).
6. Borisova T., Nazarova A., Dekaliuk M., et al. Neuromodulatory properties of fluorescent carbon dots: effect on exocytotic release, uptake and ambient level of glutamate and gaba in brain nerve terminals. Int. J. Biochem. Cell Biol., 203—215 (2015).
7. Bourdon J. A., Saber A. T., Jacobsen N. R., et al. Carbon black nanoparticle instillation induces sustained inflammation and genotoxicity in mouse lung and liver. Part. Fibre Toxicol., 1, 5 (2012).
8. Cao L., Wang X., Meziani M. J., et al. Carbon dots for multiphoton bioimaging. J. Amer. Chem. Soc., 37, 11318— 11319 (2007).
9. Chandra S., Pathan S. H., Mitra S., et al. Tuning of photoluminescence on different surface functionalized carbon quantum dots. RSC Adv., 9, 3602 (2012).
10. Chatterjee A., Wang A., Lera M., Bhattacharya S. Lunar soil simulant uptake produces a concentration-dependent increase in inducible nitric oxide synthase expression in murine raw 264.7 macrophage cells. J. Toxicol. Environ. Heal. Part A, 9, 623—626 (2010).
11. Cotman C. W. Isolation of synaptosomal and synaptic plasma membrane fractions. Methods Enzymol., 445—452 (1974).
12. Danbolt N. C. Glutamate uptake. Prog. Neurobiol., 1, 1—105 (2001).
13. Demchenko A. P., Dekaliuk M. O. Novel fluorescent carbonic nanomaterials for sensing and imaging. Methods Appl. Fluoresc., 4, 42001 (2013).
14. Dorcéna C. J., Olesik K. M., Wetta O. G., Winter J. O. Characterization and toxicity of carbon dot-poly(lacticco-glycolic acid) nanocomposites for biomedical imaging. Nano Life, 1, 1340002 (2013).
15. Esteves da Silva J. C. G., Gonçalves H. M. R. Analytical and bioanalytical applications of carbon dots. TrAC Trends Anal. Chem., 8, 1327—1336 (2011). 16. Genc S., Zadeoglulari Z., Fuss S. H., Genc K. The adverse effects of air pollution on the nervous system. J. Toxicol., 782462 (2012).
17. Jiang J., He Y., Li S., Cui H. Amino acids as the source for producing carbon nanodots: microwave assisted one-step synthesis, intrinsic photoluminescence property and intense chemiluminescence enhancement. Chem. Commun. (Camb)., 77, 9634—6 (2012).
18. Kao Y.-Y., Cheng T.-J., Yang D.-M., et al. Demonstration of an olfactory bulb-brain translocation pathway for zno nanoparticles in rodent cells in vitro and in vivo. J. Mol. Neurosci., 2, 464—71 (2012).
19. Lam C.-W., James J. T., Latch J. N., et al. Pulmonary toxicity of simulated lunar and martian dusts in mice: ii. biomarkers of acute responses after intratracheal instillation. Inhal. Toxicol., 9, 917—928 (2002).
20. Lam C.-W., James J. T., McCluskey R., et al. Pulmonary toxicity of simulated lunar and martian dusts in mice: i. histopathology 7 and 90 days after intratracheal instillation. Inhal. Toxicol., 9, 901—916 (2002).
21. Larson E., Howlett B., Jagendorf A. Artificial reductant enhancement of the lowry method for protein determination. Anal. Biochem., 2, 243—248 (1986).
22. Li H., Kang Z., Liu Y., et al. Carbon nanodots: synthesis, properties and applications. J. Mater. Chem., 46, 24230 (2012).
23. Linnarsson D., Carpenter J., Fubini B., et al. Toxicity of lunar dust Planet. Space Sci., 1, 57—71 (2012).
24. Luo P. G., Sahu S., Yang S.-T., et al. Carbon “quantum” dots for optical bioimaging. J. Mater. Chem. B, 16, 2116 (2013).
25. Mikawa M., Kato H., Okumura M., et al. Paramagnetic water-soluble metallofullerenes having the highest relaxivity for mri contrast agents. Bioconjug. Chem., 4, 510— 514 (2001).
26. Oberdörster G., Sharp Z., Atudorei V., et al. Extrapulmonary translocation of ultrafine carbon particles following whole-body inhalation exposure of rats. J. Toxicol. Environ. Heal. Part A, 20, 1531—1543 (2002).
27. Rehders M., Grosshäuser B. B., Smarandache A., et al. Effects of lunar and mars dust simulants on hacat keratinocytes and cho-k1 fibroblasts. Adv. Sp. Res., 7, 1200— 1213 (2011).
28. Roberts D. R., Albrecht M. H., Collins H. R., et al. Effects of spaceflight on astronaut brain structure as indicated on mri. N. Engl. J. Med., 18, 1746—1753 (2017).
29. Sun Y.-P., Zhou B., Lin Y., et al. Quantum-sized carbon dots for bright and colorful photoluminescence. J. Amer. Chem. Soc., 24, 7756—7757 (2006).
30. Tao H., Yang K., Ma Z., et al. In vivo nir fluorescence imaging, biodistribution, and toxicology of photoluminescent carbon dots produced from carbon nanotubes and graphite. Small, 2, 281—90 (2012).
https://doi.org/10.1002/smll.201101706
31. Wallace W. T., Taylor L. A., Liu Y., et al. Lunar dust and lunar simulant activation and monitoring. Meteorit. Planet. Sci., 7, 961—970 (2009).
32. Wang X., Qu K., Xu B., et al. Microwave assisted one-step green synthesis of cell-permeable multicolor photoluminescent carbon dots without surface passivation reagents. J. Mater. Chem., 8, 2445 (2011).
33. Zhai X., Zhang P., Liu C., et al. Highly luminescent carbon nanodots by microwave-assisted pyrolysis. Chem. Commun., 64, 7955 (2012).