DEPARTMENT OF NEUROCHEMISTRY
Head– Professor Tatiana O. Borisova, Dr.Sci. (Biol.)
Tel.:+ (044) 2343254, E-mail:
Since the establishment of the Institute of Biochemistry (1925 year), one of the main directions of scientific work was the investigation of basic biochemical mechanisms of nervous system functioning. Founder and principal leader of this research was the Director of the Institute and also Head of the Department of Biochemistry of Nervous system, Academician of the Academy of Sciences of Soviet Union and Ukraine Olexander Volodymirovich Palladin (1925 - 1972 years). Then, the neurochemical research direction in the Department was developed by Yakov Vasiliovich Belik (1973 – 1982 years); Academician of Academy of Sciences of Ukraine Valery Kazimirovich Lishko (1983 - 1991 years), Nina Germanivna Himmelreich, PhD (1991-2013 years), and Professor Tatiana Olexandrovna Borisova, Dr. Sci. (since 2013).
Nowadays, the Department of Neurochemistry consists of 12 scientists, two of them have Dr.Sci. degree
The major research of the Department is focused on molecular mechanisms of regulation of glutamatergic and GABAergic neurotransmission; exocytosis; neurodegeneration; neurotoxicity risk assessment; the cellular basis of synaptopathy; neuronal plasticity and neuroprotection. Current research addresses the problems of basic and applied neuroscience, including regulation of vesicular and transporter-dependent transport of neurotransmitters (glutamate, GABA, aspartate, glycine), effects of activation of presynaptic glutamate and GABA receptors, modulation of lipid composition of the plasma membrane, planar lipid bilayer studies, neurotoxicity risk assessment, effects of heavy metals, investigation of glutamate transport in blood platelets. Also, four current projects related to cellular biotechnology and space–related research are funded by NAS of Ukraine. Glutamate transport in blood platelets (as peripheral model of presynapse) is also of interest because of the possibility of early diagnostic of alterations in glutamate transport in the brain.
Methods: radioisotope analysis, fluorescence spectroscopy, laser correlation spectroscopy, confocal microscopy, flow cytometry, the method of registration ionic conductivity planar bilayer lipid membrane, cell-free system to study exocytosis, and animal experimental models, that is, perinatal hypoxia accompanied by convulsions; special centrifuge-induced hypoxia, cholesterol deficiency, vitamin D deficiency, etc.
Main scientific achievements in 2010-2015 years
The burden of the modern society is a continuous increase in the number of patients with neurological and neurodegenerative disorders. Nowadays, the analysis of the role of cholesterol in brain functioning is of paramount importance and probably will be so for a long time. The main question addressed was whether membrane cholesterol modulated glutamate transport in presynaptic nerve terminals, and whether altered cholesterol composition of neuronal membrane could mediate pathogenic mechanisms responsible for neurodegeneration or vice versa have neuroprotective features. Cholesterol depletion with methyl--cyclodextrin (MCD) acutely applied to rat brain synaptosomes is accompanied by an immediate increase in transporter-mediated glutamate release and a decrease in exocytotic release. The application of MCD to synaptosomes, as well as to isolated synaptic vesicles, led to the gradual leakage of the protons from the vesicles, whereas the application of MCD complexed with cholesterol stimulated additional vesicle acidification and an increase in Ca2+-dependent exocytotic response. The treatment of nerve terminals with MCD did not block Ca2+-triggered vesicle recycling. Cholesterol depletion of the plasma membrane with MCD induces the removal of cholesterol from the membrane of synaptic vesicles resulting in immediate dissipation of synaptic vesicle proton gradient and redistribution of the neurotransmitter between the vesicular and cytosolic pools. The latter appears to be the main cause of a dramatic decrease in exocytotic and considerable increase in transporter-mediated release of L-[14C]glutamate.
The low level of ambient glutamate is extremely important for proper spontaneous activity and synaptic transmission in the brain. It was examined whether membrane cholesterol modulated the extracellular glutamate level in the nerve terminals and the processes responsible for its maintenance. The ambient glutamate level, being equilibrium between Na+-dependent uptake and tonic release, was increased in rat brain synaptosomes treated with MCD. Also, cholesterol-deficient synaptosomes showed a lower initial velocity of glutamate uptake. In the presence of competitive non-transportable inhibitor of glutamate transporters DL-threo--benzyloxyaspartate, which significantly reduced glutamate uptake, net tonic release of glutamate from cholesterol-depleted synaptosomes was decreased. It was suggested that cholesterol deficiency altered the intra-to-extracellular glutamate ratio by the reduction of the cytosolic level and the augmentation of the ambient level of the neurotransmitter, thereby favoring a decrease in tonic glutamate release. Thus, increased extracellular concentration of glutamate in cholesterol - deficient nerve terminals was not a result of the changes in tonic release (and/or glutamine synthetase activity), but was set by lack function of glutamate transporters.
In cerebral hypoxia/ischemia, stroke, traumatic brain injury, the development of neurotoxocity is provoked by enhanced extracellular glutamate, which is released from nerve cells mainly by glutamate transporter reversal − a distinctive feature of these pathological states. Transporter-mediated glutamate release from the synaptosomes: 1) stimulated by depolarization of the plasma membrane; 2) by means of heteroexchange with competitive transportable inhibitor of glutamate transporters DL-threo--hydroxyaspartate; 3) in low [Na+] medium; and 4) during dissipation of the proton gradient of synaptic vesicles by the protonophore carbonyl cyanide-p-trifluoromethoxyphenyl-hydrazon; was decreased under the conditions of cholesterol deficiency. Thus, a decrease in the level of membrane cholesterol attenuated transporter-mediated glutamate release from the nerve terminals. Therefore, lowering cholesterol may be used in neuroprotection in ischemia, stroke, traumatic brain injury that are associated with an increase in glutamate uptake reversal. This data can explain the neuroprotective effects of statins in these pathological states and provide one of the mechanisms of their neuroprotective action. However, beside these disorders lowering cholesterol may cause harmful consequences decreasing glutamate uptake by the nerve terminals.
Perinatal hypoxia leads to multiple chronic neurological deficits including mental retardation, learning and memory disabilities, behavioral abnormalities and epilepsy. The effects of highly selective blocker GAT1, NO-711, and substrate inhibitor GAT3, β-alanine, on the initial velocity of [3H]GABA uptake by cortical, hippocampal and thalamic nerve terminals were analyzed after perinatal hypoxia. Rats underwent to hypoxia and seizures at the age of 10-12 postnatal days and used in the experiments 8-9 weeks after hypoxia. The effectiveness of β-alanine to influence GABA uptake increased in hippocampal and thalamic nerve terminals as a result of perinatal hypoxia, whereas the capacity of NO-711 in thalamic nerve terminals decreased. These results may indicate changes in the ratio of active GAT1/GAT3 expressed in the plasma membrane of nerve terminals after perinatal hypoxia. A principal possibility of non-GAT1-targeting modulation of GABA transporter activity in different brain regions by exogenous and endogenous β-alanine was suggested.
Positive allosteric modulators of GABAB receptors have great therapeutic potential for medications of anxiety, depression, etc. The effects of recently discovered modulator rac-BHFF on the key characteristics of GABAergic neurotransmission were investigated in cortical and hippocampal presynaptic nerve terminals. The ambient level of [3H]GABA that is a balance between release and uptake of the neurotransmitter increased significantly in the presence of rac-BHFF. The initial velocity of synaptosomal [3H]GABA uptake was suppressed by the modulator. In the presence of GABA transporter blocker NO-711, it was shown that rac-BHFF increased tonic release of [3H]GABA from synaptosomes. Rac-BHFF did not enhance inhibiting effect of (±)-baclofen on depolarization-induced exocytotic release of [3H]GABA. Rac-BHFF caused dose-dependent depolarization of the plasma membrane and dissipation of the proton gradient of synaptic vesicles in synaptosomes that was shown in the absence/presence of GABAB receptor antagonist saclofen using fluorescent dyes rhodamine 6G and acridine orange, respectively, and so, above effects of rac-BHFF were not associated with modulation of presynaptic GABAB receptors. Therefore, drug development strategy of positive allosteric modulation of GABAB receptors is to eliminate above side effects of rac-BHFF in presynapse, and vice versa, these new properties of rac-BHFF may be exploited appropriately.
Fluorinated analogues of natural substances take an essential place in the design of new biologically active compounds. The effects of synthesized β-polyfluoroalkyl-GABAs (FGABAs) on [3H]GABA uptake by isolated rat brain nerve terminals were assessed and compared with those of Pregabalin. FGABAs did not influence the initial velocity of [3H]GABA uptake when applied acutely, whereas an increase in this parameter was found after preliminary incubation of FGABAs with synaptosomes. Pregabalin after preliminary incubation with synaptosomes caused unidirectional changes in the initial velocity of [3H]GABA uptake. Using specific inhibitors of GAT1 and GAT3, NO-711 and SNAP5114, respectively, the ability of FGABAs to influence non-GAT1 and non-GAT3 uptake activity of nerve terminals was analysed, but no specificity was found. Therefore, new synthesized FGABAs are structural but not functional analogues of GABA (because they did not inhibit synaptosomal [3H]GABA uptake). Moreover, FGABAs are able to increase the initial velocity of [3H]GABA uptake by synaptosomes, and this effect is higher than that of Pregabalin.
The production of reactive oxygen species (ROS) as a response to presynaptic glutamate receptor activation, and the role of ROS in neurotransmitter (GABA) release was investigated. Experiments were performed with rat brain cortical synaptosomes using glutamate, NMDA and kainate as agonists of glutamate receptors. ROS production was evaluated with the fluorogenic compound dichlorodihydrofluorescein diacetate (H(2)DCF-DA), and GABA release was studied using synaptosomes loaded with [(3)H]GABA. All agonists were found to stimulate ROS production, and specific antagonists of NMDA and kainate/AMPA receptors, dizocilpine hydrogen maleate (MK-801) and 6-cyano-7-nitroquinoxaline-2,3-done (CNQX), significantly inhibited the ROS increase. Spontaneous as well as agonist-evoked ROS production was effectively attenuated by diphenyleneiodonium (DPI), a commonly used potent inhibitor of NADPH oxidase activity, that suggests a high contribution of NADPH-oxidase to this process. The replacement of glucose with pyruvate or the simultaneous presence of both substrates in the medium led to the decrease in spontaneous and NMDA-evoked ROS production, but to the increase in ROS production induced by kainate. Scavenging of agonist-evoked ROS production by a potent antioxidant N-acetylcysteine was tightly correlated with the inhibition of agonist-evoked GABA release. Together, these findings show that the activation of presynaptic glutamate receptors induces an increase in ROS production, and there is a tight correlation between ROS production and GABA secretion. The pivotal role of kainate/AMPA receptors in ROS production is under discussion.
New insights into molecular mechanism(s) underlying the presynaptic action of nitric oxide on GABA release were proposed. Nitric oxide (NO) is an important presynaptic modulator of synaptic transmission. Diethylamine NONOate (DEA/NO) and S-nitroso-N-acetylpenicillamine (SNAP) were used as NO donors. DEA/NO and SNAP (in the presence of dithiothreitol (DTT)) stimulated external Ca2 +-independent [3H]GABA release, which was not attributed to a rise in intracellular calcium concentration. [3H]GABA release coincided with increasing GABA level in cytosol and decreasing the vesicular GABA content available for exocytotic release. There was a strong temporal correlation between NO-induced increase in cytosolic [GABA] and dissipation of both synaptic vesicle proton gradient and mitochondrial membrane potential. Dissipation was reversible, and recovery of both parameters correlated in time with re-accumulation of [3H]GABA into synaptic vesicles. The molar ratio of DTT to SNAP determined the rate and duration of the recovery processes.We suggest that NO can stimulate GABA release via GABA transporter reversal resulting from increased GABA levels in cytosol. The latter is reversible and appears to be due to S-nitrosylation of key proteins, which affect the energy status of the pre-synapse.Our findings provide new insight into molecular mechanism(s) underlying the presynaptic action of nitric oxide on inhibitory neurotransmission.
The action of calix[4]arenes C-91, C-97, C-99, C-107 and C-160 on solvent-containing planar bilayer membranes made of cholesterol and egg phosphatidylcholine (egg PC) or synthetic 18-carbon-tail phospholipid DOPC has been investigated in a voltage-clamp mode. Within the range of calix[4]arenes tested, a steady-state voltage-dependent transmembrane current was achieved only after addition of calix[4]-arene C-99 (calix[4]arene-bis-hydroxymethylphosphonic acid) from the side of the membrane the positive potential was applied to. This current exhibited anion selectivity passing more chloride at negative potentials applied from the side of the membrane to which calix[4]arene C-99 was introduced. The kinetics and temperature-dependence determined for calix[4]arene C-99-mediated ionic transport suggest a carrier mode of facilitated diffusion.
Carbon dots (C-dots), a recently discovered class of fluorescent nano-sized particles with pure carbon core, have great bioanalytical potential. Neuroactive properties of fluorescent C-dots obtained from β-alanine by microwave heating were assessed based on the analysis of their effects on the key characteristics of GABA- and glutamatergic neurotransmission in isolated rat brain nerve terminals. It was found that C-dots in dose-dependent manner: (1) decreased exocytotic release of [3H]GABA and L-[14C]glutamate; (2) reduced acidification of synaptic vesicles; (3) attenuated the initial velocity of Na+-dependent transporter-mediated uptake of [3H]GABA and L-[14C]glutamate; (4) increased the ambient level of the neurotransmitters, nevertheless (5) did not change significantly the potential of the plasma membrane of nerve terminals. Fluorescent and neuromodulatory features combined in C-dots create base for their potential usage for labeling and visualization of key processes in nerve terminals, and also in theranostics. In addition, natural presence of carbon-containing nanoparticles in the human food chain and in the air may provoke the development of neurologic consequences.
Platelets express neuronal and glial glutamate transporters EAAT 1-3 in the plasma membrane and vesicular glutamate transporters VGLUT 1,2 in the membrane of secretory granules. This study is focused on the assessment of non-exocytotic glutamate release, that is, the unstimulated release, heteroexchange and glutamate transporter reversal in platelets. Using the glutamate dehydrogenase assay, the absence of unstimulated release of endogenous glutamate from platelets was demonstrated, even after inhibition of glutamate transporters and cytoplasmic enzyme glutamine synthetase by DL-threo--benzyloxyaspartate and methionine sulfoximine, respectively. Depolarization of the plasma membrane by exposure to elevated [K+] did not induce the release of glutamate from platelets that was shown using the glutamate dehydrogenase assay and radiolabeled L-[14C]glutamate. Glutamate efflux by means of heteroexchange with transportable inhibitor of glutamate transporters DL-threo--hydroxyaspartate (DL-THA) was not observed. Furthermore, the protonophore cyanide-p-trifluoromethoxyphenyl-hydrazon (FCCP) and inhibitor of V-type H+-ATPase bafilomycin A1 also failed to stimulate the release of glutamate from platelets. However, exocytotic release of glutamate from secretory granules in response to thrombin stimulation was not prevented by elevated [K+], DL-THA, FCCP and bafilomycin A1. In contrast to nerve terminals, platelets cannot release glutamate in a non-exocytotic manner. Heteroexchange, transporter-mediated and unstimulated release of glutamate are not inherent to platelets. Therefore, platelets may be used as a peripheral marker/model for the analysis of glutamate uptake by brain nerve terminals only (direct function of transporters), whereas the mechanisms of glutamate release are different in platelets and nerve terminals. Glutamate is released by platelets exclusively by means of exocytosis. Also, reverse function of vesicular glutamate transporters of platelets is rather ambiguous.
Diabetic neuropathy represents one of the most prevalent complications of diabetes mellitus. The aim of this study was to investigate the effect of diabetes-induced disturbances in neurons on the Ca(2+)-triggered membrane fusion process in cell-free system in relation to plasmalemma cholesterol level. The diabetes in rats was induced by streptozotocin. After 4 weeks of diabetes induction the one group of diabetic rats was treated with gabapentin. Fusion experiments were performed in the cell-free model system using fluorescent dye octadecylrhodamine B. The synaptosomal plasma membrane cholesterol level in diabetic rats was higher than in control and was decreased after gabapentin therapy. The rate of synaptic vesicles fusion with plasma membranes in the presence of Ca(2+) and synaptosomal cytosolic proteins was decreased in diabetic rats as compared to control (and after gabapentin administration to diabetic rats was raised. At diabetes the stimulated synaptosomal serotonin release was increased in 1.7-2 folds and was partially normalized by gabapentin therapy. Together, these findings suggest that elevated cholesterol content in neuronal plasma membranes at diabetes impairs the membrane fusion process in neurons that can induce the development of neuropathy. Diabetes-evoked impairments of the exocytotic process can be attenuated by gabapentin therapy.
Since 2010, 4 Ukrainian patents were obtained.
Since 2010, two the sisdefense for Doctor Degree and four - Ph.D. were held in the Department.
{spoiler title=Publications opened=1}
2010
1. Borisova T., Krisanova N., Sivko R., Borysov A. Cholesterol depletion attenuates tonic release but increases the ambient level of glutamate in rat brain synaptosomes. // Neurochemistry Int. - 2010. - Vol. 56. № 3. - Р. 466-478.
2. Kasatkina L., Borisova T. Impaired Na+- dependent glutamate uptake in platelets during depolarization of their plasma membrane. // Neurochemistry Int. - 2010. - Vol. 56, № 5. - Р. 711-719.
3. Tarasenko A.S., Sivko R.V.,.Krisanova N.V, Himmelreich N.H., Borisova T.A. Cholesterol depletion from the plasma membrane impairs proton and glutamate storage in synaptic vesicles of nerve terminals/ // Journal of Molecular Neuroscience. - 2010. - Vol. 41, № 3. - Р. 358-367.
4. Borisova T., Sivko R., Borysov A., Krisanova N. Diverse presynaptic mechanisms underlying methyl-beta-cyclodextrin – mediated changes in glutamate transport. // Cellular and Molecular Neurobiology.- 2010.- Vol.30, № 7.- Р. 1013-1023.
5. Крупко О. А., Тарасенко А.С., Гиммельрейх Н.Г. Механизмы модуляторного влияния экзогенного глутамата на процессы секреции в гиппокампальных пресинаптических терминалях. // Нейрофизиология, - 2010. - Т. 42, № 2. - С.101-111.
6. Trikash I., Gumenyuk V., Lishko V. The fusion of synaptic vesicle membranes studied by lipid mixing: the R18 fluorescence assay validity. // Chemistry and Physics of Lipids, – 2010. – Vol. 163, №8. - Р. 778–786.
2011
7. Borisova T., Kasatkina L., Ostapchenko L. The proton gradient of secretory granules and glutamate transport in blood platelets during cholesterol depletion of the plasma membrane by methyl-beta-cyclodextrin. // Neurochemistry Int.- 2011. - Vol. 59, № 6. - Р. 965-975.
8. Borisova T., Krisanova N., Sivko R., Kasatkina L., Borysov A., Griffin S., Wireman M. Presynaptic malfunction: The neurotoxic effects of cadmium and lead on the proton gradient of synaptic vesicles and glutamate transport.// Neurochemistry Int. - 2011 .- Vol. 59, № 2.- Р. 272-279.
9. Борисова Т., Дудченко Н., Брик О., Касаткина Л., Сивко Р., Чунихин А., Крысанова Н. Взаимодействие наночастиц магнетита, покрытых полимерами, с нервными терминалами головного мозга и тромбоцитами крови. // Биотехнология, -2011. - Т.4, № 5, - С. 45-56.
10. Pozdnyakova N., Yatsenko L., Parkhomenko N. Himmelreich N. Perinatal hypoxia induces long-lasting increase in unstimulated GABA release in rat brain cortex and hippocampus. The protective effect of pyruvate. // Neurochem.Int. – 2011. - Vol. 58, № 1. - Р. 14-21.
11. Tarasenko A., Krupko O., Himmelreich N. Presynaptic kainate and NMDA receptors are implicated in the modulation of GABA release from cortical and hippocampal nerve terminals. // Neurochemistry Int. – 2011. - Vol. 59, № 1. - P. 81-89.
12. Dunne M., Sadhukhan A., Rehders M., Brix K., Vogt P. M., Jokuszies A., Mirastschijski U., Borisova T., Slenzka K., Vogt J., Rettberg P., Rabbow E. Effects of different space relevant environmental stressors including Lunar Dust on microorganisms and human cells of different tissues. // 40th International Conference on Environmental Systems, Published by the American Institute of Aeronautics and Astronautics, Inc., AIAA 2010-6076. – 2010. – P.1-21.
2012
13. Krisanova N., Sivko R., Kasatkina L., Borisova T. Neuroprotection by lowering cholesterol: A decrease in membrane cholesterol content reduces transporter-mediated glutamate release from brain nerve terminals. // Biochim. Biophys. Acta, - 2012. - Vol.1822, № 10. - Р. 1553–1561.
14. Yatsenko L., Pozdnyakova N., Dudarenko M., Himmelreich N. The dynamics of changes in hippocampal GABAergic system in rats exposed to early-life hypoxia-induced seizures // Neurosci. Lett. - 2012.- Vol. 524, № 2. - P.69-73
15. A. Tarasenko, O. Krupko, N. Himmelreich Reactive oxygen species induced by presynaptic glutamate receptor activation are involved in [3H]GABA release from rat brain cortical nerve terminals. // Neurochemistry Int. – 2012. - Vol. 61, № 7. - P. 1044-1051.
2013
16. Gumenyuk V.P., Chunikhin A.Ju., Himmelreich N.H., Trikash I.O. The phenomenon of synaptic vesicle clustering as the prefusion state in the model system of exocytosis. // General Physiology and Biophysics, – 2013. – Vol. 4, № 32. - Р. 545-558.
17. Kasatkina L, Borisova T. Glutamate release from platelets: Exocytosis versus glutamate transporter reversal. // Int.J. Biochem.Cell Biol. – 2013. – Vol. 45, № 11. - P. 2585-2595.
18. Krisanova N., Kasatkina L, Sivko R, Borysov A, Nazarova A, Slenzka K, Borisova T. Neurotoxic potential of lunar and martian dust: influence on em, proton gradient, active transport, and binding ofglutamate in rat brain nerve terminals. // Astrobiology, - 2013. – Vol.13, № 8. - P. 679-692.
19. Borisova T. Cholesterol and presynaptic glutamate transport in the brain. Springer, Book Series «Springer Briefs in Neuroscience», (2013) 76 p. (ISBN 978-1-4614-7758-7) (DOI 10.1007/978-1-4614-7759-4).
2014
20. Krisanova N., Sivko R., Kasatkina L., Borуsov A., Borisova T. Excitotoxic potential of exogenous ferritin and apoferritin: Changes in ambient level of glutamate and synaptic vesicle acidification in brain nerve terminals. // Cell.Mol. Neuroscience. – 2014. – 58.– P.95-104.
21. O.Ya. Shatursky, L.A. Kasatkina, R.V. Rodik, S.O. Cherenok, A.A. Shkrabak, T.O. Veklich, T.A. Borisova, S.O. Kosterin and Vitaly I. Kalchenko. Anion carrier formation by calix[4]arene-bis-hydroxymethylphosphonic acid in bilayer membranes // Organic & Biomolecular Chemistry. 2014 – 12-P. 9811-9821.
22. Tarasenko A, Krupko O, Himmelreich N. New insights into molecular mechanism(s) underlying the presynaptic action of nitric oxide on GABA release.// Biochim Biophys Acta. – 2014. – 1840(6) – P.1923-1932.
23. Borisova T., Krisanova N., Borуsov A., Sivko R., Ostapchenko L., Babic M., Horak D. Manipulation of brain nerve terminals by an external magnetic field using D-mannose-coated γ-Fe2O3 nano-sized particles and their effects on glutamate transport. // Beilstein J. Nanotechnol. – 2014. – 5.– P.778-788.
24. O.Ya. Shatursky, O.V. Romanenko, N.G. Himmelreich. Long open amphotericin channels revealed in cholesterol-containing phospholipid membranes are blocked by thiazole derivative // J. Membrane Biol. 2014. – 247:211-229.
25. N. Pozdnyakova, M. Dudarenko, L. Yatsenko, N. Himmelreich, O. Krupko, T. Borisova Perinatal hypoxia: different effects of the inhibitors of GABA transporters GAT1 and GAT3 on the initial velocity of [3H]GABA uptake by cortical, hippocampal, and thalamic nerve terminals.// Croat Med J. 2014;55:250-8
26. A. Borysov, N. Krisanova, O. Chunihin, L. Ostapchenko, N. Pozdnyakova, Т. Borisova A comparative study of neurotoxic potential of synthesized polysaccharidecoated and native ferritinbased magnetic nanoparticles.// Croat Med J. 2014;55:195-205.
27. V. P. Gumenyuk, I. O. Trikash Effects of Levetiracetam on Aggregation and Fusion of Membranes of Synaptic Vesicles in a Cell-Free Exocytosis Model //Neurophysiology, – 2014, – 46, 2, P. 115-119.
2015
28. O. Soldatkin, A. Nazarova, N. Krisanova, A. Borуsov, D. Kucherenko, I. Kucherenko, N. Pozdnyakova, A. Soldatkin, T. Borisova Monitoring of the velocity of high-affinity glutamate uptake by isolated brain nerve terminals using amperometric glutamate biosensor //Talanta -2015-V 135.-P. 67–74.
29. Borisova T, Nazarova A, Dekaliuk M, Krisanova N, Pozdnyakova N, Borysov A, Sivko R, Demchenko AP. 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. -2015.-V.59-P.203-15.{/spoiler}