Evaluation of the potential neuroactivity in the brain nerve terminals of the C60 fullerene planetary dust component
Heading:
| 1Krisanova, NV, 1Dudarenko, MV, 1Pastukhov, AO, 1Sivko, RV, 1Kalynovska, LM, 1Driuk, MM, 1Nazarova, AG, 1Gutich, IІ, 1Shliakhovyi, VV, 1Pozdnyakova, NG 1Palladin Institute of Biochemistry of National Academy of Sciences of Ukraine, Kyiv, Ukraine |
| Space Sci. & Technol. 2023, 29 ;(5):060-068 |
| https://doi.org/10.15407/knit2023.05.060 |
| Publication Language: Ukrainian |
Abstract: A study of the infrared spectrum of the environment of the planetary nebula Tc 1 revealed the radiation of cold and neutral fullerenes C60 and C70. The results of the analysis of infrared spectra obtained using the Hubble space telescope conclusively proved the existence of C60+ fullerene in the interstellar medium. These large carbon-containing molecules can form and exist in the interstellar medium and are candidates to explain many diffuse interstellar absorption bands.
In this study, the potential neuroactivity of the C60 fullerene as a planetary dust component was assessed in the isolated rat brain nerve terminals. It was shown that C60 fullerene in the unirradiated state at concentrations of 0.05¾0.25 mg/ml did not change the extracellular levels of excitatory neurotransmitter L-[14C]glutamate and inhibitory neurotransmitter [3H]GABA in the preparations of rat brain nerve terminals. An increase in fullerene C60 concentrations up to 0.5 and 1.00 mg/ml was accompanied by an increase in the extracellular levels of L-[14C]glutamate and [3H]GABA in the preparations of nerve terminals. Therefore, fullerene C60 did not cause signs of acute neurotoxicity in the brain nerve terminals within the concentration range of 0.05¾0.25 mg/ml. However, given that C60 undergoes photooxidation, it can be expected that it may acquire neurotoxic properties in situ.
|
| Keywords: brain nerve terminals, extracellular neurotransmitter levels, fullerene C60, L-[14C]glutamate, planetary dust, synaptosomes, [3H]GABA |
References:
1. Abbott N.J. (2000). Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol. V.20, № 2, P. 131-147.
https://doi.org/10.1023/A:1007074420772
2. Aly F.M., Othman A., Haridy M.A.M. (2018). Protective Effects of Fullerene C60 Nanoparticles and Virgin Olive Oil against Genotoxicity Induced by Cyclophosphamide in Rats Oxid. Med. Cell. Longev. V.2018,
https://doi.org/10.1155/2018/1261356
3. Baati T., Bourasset F., Gharbi N., et al. (2012). The prolongation of the lifespan of rats by repeated oral administration of [60]fullerene Biomaterials. V.33, № 19, P. 4936-4946.
https://doi.org/10.1016/j.biomaterials.2012.03.036
4. Borisova T. (2016). Permanent dynamic transporter-mediated turnover of glutamate across the plasma membrane of presynaptic nerve terminals: arguments in favor and against. Rev. Neurosci. V.27, № 1, P. 71-81.
https://doi.org/10.1515/revneuro-2015-0023
DOI: 10.1515/revneuro-2015-0023.
https://doi.org/10.1515/revneuro-2015-0023
5. Borisova T. (2018). Nervous System Injury in Response to Contact With Environmental, Engineered and Planetary Micro- and Nano-Sized Particles Front. Physiol. V.9, P. 728.
https://doi.org/10.3389/fphys.2018.00728
6. Borisova T. (2019). Express assessment of neurotoxicity of particles of planetary and interstellar dust npj Microgravity. V.5, № 1, P. 2.
https://doi.org/10.1038/s41526-019-0062-7
7. Borisova T., Borysov A. (2016). Putative duality of presynaptic events. Rev. Neurosci. V.27, № 4, P. 377-83.
https://doi.org/10.1515/revneuro-2015-0044
8. Borisova T., Kucherenko D., Soldatkin O., et al. (2018). An amperometric glutamate biosensor for monitoring glutamate release from brain nerve terminals and in blood plasma Anal. Chim. Acta. V.1022, P. 113-123.
https://doi.org/10.1016/j.aca.2018.03.015
9. Borisova T., Pozdnyakova N., Dudarenko M., et al. (2021). GABAA receptor agonist cinazepam and its active metabolite 3-hydroxyphenazepam act differently at the presynaptic site Eur. Neuropsychopharmacol. V.45, P. 39-51.
https://doi.org/10.1016/j.euroneuro.2021.03.013
10. Borisova T., Pozdnyakova N., Krisanova N., et al. (2021). Unique features of brain metastases-targeted AGuIX nanoparticles vs their constituents: A focus on glutamate-/GABA-ergic neurotransmission in cortex nerve terminals Food Chem. Toxicol. V.149, P. 112004.
https://doi.org/10.1016/j.fct.2021.112004
11. Borisova T., Pozdnyakova N., Shaitanova E., et al. (2015). Synthesis of new fluorinated analogs of GABA, Pregabalin bioisosteres, and their effects on [3H]GABA uptake by rat brain nerve terminals Bioorg. Med. Chem. V.23, № 15, P. 4316-4323.
https://doi.org/10.1016/j.bmc.2015.06.038
12. Borysov A., Krisanova N., Chunihin O., et al. (2014). A comparative study of neurotoxic potential of synthesized polysaccharide-coated and native ferritin-based magnetic nanoparticles. Croat. Med. J. V.55, № 3, P. 195-205.
https://doi.org/10.3325/cmj.2014.55.195
13. Bourdon J.A., Saber A.T., Jacobsen N.R., et al. (2012). Carbon black nanoparticle instillation induces sustained inflammation and genotoxicity in mouse lung and liver V.9, № 1, P. 5.
https://doi.org/10.1186/1743-8977-9-5
14. Cami J., Bernard-Salas J., Peeters E., et al. (2010). Detection of C60 and C70 in a young planetary nebula Science. V.329, № 5996, P. 1180-1182.
https://doi.org/10.1126/science.1192035
15. Campbell E.K., Holz M., Gerlich D., et al. (2015). Laboratory confirmation of C60(+) as the carrier of two diffuse interstellar bands Nature. V.523, № 7560, P. 322-323.
https://doi.org/10.1038/nature14566
16. Chatterjee A., Wang A., Lera M., et al. (2010). 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. V.73, № 9, P. 623-626.
https://doi.org/10.1080/15287390903578182
17. Cordiner M.A., Linnartz H., Cox N.L.J., et al. (2019). Confirming Interstellar C60+ Using the Hubble Space Telescope Astrophys. J. Lett. V.875, № 2, P. L28.
https://doi.org/10.3847/2041-8213/ab14e5
18. Cotman C.W. (1974). Isolation of synaptosomal and synaptic plasma membrane fractions. Methods Enzymol. V.31, P. 445-452.
https://doi.org/10.1016/0076-6879(74)31050-6
19. Evans A., Loon J.T. van, Woodward C.E., et al. (2012). Solid-phase C60 in the peculiar binary XX Oph Mon. Not. R. Astron. Soc. Lett. V.421, № 1, P. L92-L96.
https://doi.org/10.1111/j.1745-3933.2012.01213.x
20. Friedman S.H., DeCamp D.L., Kenyon G.L., et al. (1993). Inhibition of the HIV-1 protease by fullerene derivatives: model building studies and experimental verification J. Am. Chem. Soc. V.115, № 15, P. 6506-6509.
https://doi.org/10.1021/ja00068a005
21. Huang Y.Y., Sharma S.K., Yin R., et al. (2014). Functionalized Fullerenes in Photodynamic Therapy J. Biomed. Nanotechnol. V.10, № 9, P. 1918.
https://doi.org/10.1166/jbn.2014.1963
22. Juha L., Krása J., Láska L., et al. (1993). Fast degradation of fullerenes by ultraviolet laser radiation Appl. Phys. B Photophysics Laser Chem. V.57, № 1, P. 83-84.
https://doi.org/10.1007/BF00324103
23. Krisanova N., Kasatkina L., Sivko R., et al. (2013). Neurotoxic Potential of Lunar and Martian Dust: Influence on Em, Proton Gradient, Active Transport, and Binding of Glutamate in Rat Brain Nerve Terminals Astrobiology. V.13, № 8, P. 679-692.
https://doi.org/10.1089/ast.2012.0950
24. Krisanova N. V., Trikash I.O., Borisova T.A. (2009). Synaptopathy under conditions of altered gravity: changes in synaptic vesicle fusion and glutamate release Neurochem. Int. V.55, № 8, P. 724-731.
https://doi.org/10.1016/j.neuint.2009.07.003
25. Larson E., Howlett B., Jagendorf A. (1986). Artificial reductant enhancement of the Lowry method for protein determination. Anal. Biochem. V.155, № 2, P. 243-248.
https://doi.org/10.1016/0003-2697(86)90432-X
26. Liu J., Ohta S. ichi, Sonoda A., et al. (2007). Preparation of PEG-conjugated fullerene containing Gd3+ ions for photodynamic therapy J. Control. Release. V.117, № 1, P. 104-110.
https://doi.org/10.1016/j.jconrel.2006.10.008
27. Maeda-Mamiya R., Noiri E., Isobe H., et al. (2010). In vivo gene delivery by cationic tetraamino fullerene Proc. Natl. Acad. Sci. U. S. A. V.107, № 12, P. 5339-5344.
https://doi.org/10.1073/pnas.0909223107
DOI: 10.1073/PNAS.0909223107/ASSET/30D5E1E2-9A10-4F23-9643-2EE45DA03CBA/ASSETS/GRAPHIC/PNAS.0909223107EQ2.GIF.
28. Markovic Z., Trajkovic V. (2008). Biomedical potential of the reactive oxygen species generation and quenching by fullerenes (C60) Biomaterials. V.29, № 26, P. 3561-3573.
https://doi.org/10.1016/j.biomaterials.2008.05.005
29. Pozdnyakova N., Krisanova N., Dudarenko M., et al. (2020). Inhibition of sigma-1 receptors substantially modulates GABA and glutamate transport in presynaptic nerve terminals Exp. Neurol. V.333,
https://doi.org/10.1016/j.expneurol.2020.113434
30. Pozdnyakova N., Pastukhov A., Dudarenko M., et al. (2016). Neuroactivity of detonation nanodiamonds: dose-dependent changes in transporter-mediated uptake and ambient level of excitatory/inhibitory neurotransmitters in brain nerve terminals J. Nanobiotechnology. V.14, № 1, P. 25.
https://doi.org/10.1186/s12951-016-0176-y
31. Quick K.L., Ali S.S., Arch R., et al. (2008). A carboxyfullerene SOD mimetic improves cognition and extends the lifespan of mice Neurobiol. Aging. V.29, № 1, P. 117-128.
https://doi.org/10.1016/j.neurobiolaging.2006.09.014
32. Rehders M., Grosshäuser B.B., Smarandache A., et al. (2011). Effects of lunar and mars dust simulants on HaCaT keratinocytes and CHO-K1 fibroblasts Adv. Sp. Res. V.47, № 7, P. 1200-1213.
https://doi.org/10.1016/j.asr.2010.11.033
33. Rouse J.G., Yang J., Ryman-Rasmussen J.P., et al. (2007). Effects of mechanical flexion on the penetration of fullerene amino acid-derivatized peptide nanoparticles through skin Nano Lett. V.7, № 1, P. 155-160.
https://doi.org/10.1021/nl062464m
34. Santos S.M., Dinis A.M., Peixoto F., et al. (2014). Interaction of fullerene nanoparticles with biomembranes: from the partition in lipid membranes to effects on mitochondrial bioenergetics Toxicol. Sci. V.138, № 1, P. 117-129.
https://doi.org/10.1093/toxsci/kft327
35. Shershakova N., Baraboshkina E., Andreev S., et al. (2016). Anti-inflammatory effect of fullerene C60 in a mice model of atopic dermatitis J. Nanobiotechnology. V.14, № 1, P. 1-11.
https://doi.org/10.1186/s12951-016-0159-z
DOI: 10.1186/S12951-016-0159-Z/TABLES/2.
36. Soldatkin O., Nazarova A., Krisanova N., et al. (2015). Monitoring of the velocity of high-affinity glutamate uptake by isolated brain nerve terminals using amperometric glutamate biosensor. Talanta. V.135, P. 67-74.
https://doi.org/10.1016/j.talanta.2014.12.031
DOI: 10.1016/j.talanta.2014.12.031.
https://doi.org/10.1016/j.talanta.2014.12.031
37. Sun Y.P., Ma B., Bunker C.E., et al. (1995). All-carbon polymers (polyfullerenes) from photochemical reactions of fullerene clusters in room-temperature solvent mixtures J. Am. Chem. Soc. V.117, № 51, P. 12705-12711.
https://doi.org/10.1021/ja00156a007
38. Taylor R., Parsons J.P., Avent A.G., et al. (1991). Degradation of C60 by light Nat. 1991 3516324. V.351, № 6324, P. 277-277.
https://doi.org/10.1038/351277a0
39. Tsuchiya T., Oguri I., Yamakoshi Y.N., et al. (1996). Novel harmful effects of [60]fullerene on mouse embryos in vitro and in vivo FEBS Lett. V.393, № 1, P. 139-145.
https://doi.org/10.1016/0014-5793(96)00812-5
40. Wallace W.T., TAYLOR L.A., LIU Y., et al. (2009). Lunar dust and lunar simulant activation and monitoring Meteorit. Planet. Sci. V.44, № 7, P. 961-970.
https://doi.org/10.1111/j.1945-5100.2009.tb00781.x
41. Yin J.J., Lao F., Fu P.P., et al. (2009). The scavenging of reactive oxygen species and the potential for cell protection by functionalized fullerene materials Biomaterials. V.30, № 4, P. 611.
https://doi.org/10.1016/j.biomaterials.2008.09.061
42. Zakharian T.Y., Seryshev A., Sitharaman B., et al. (2005). A fullerene-paclitaxel chemotherapeutic: synthesis, characterization, and study of biological activity in tissue culture J. Am. Chem. Soc. V.127, № 36, P. 12508-12509.
https://doi.org/10.1021/ja0546525