ДВОЙСТВЕННЫЕ ТРАНСДУКЦИОННЫЕ ФУНКЦИИ НЕЙРОНАЛЬНЫХ ГЛУТАМАТНЫХ РЕЦЕПТОРОВ N-МЕТИЛ-D-АСПАРТАТА И ИХ РОЛЬ В ФИЗИОЛОГИИ И ПАТОЛОГИИ ГОЛОВНОГО МОЗГА
Аннотация
В этом обзоре проанализированы два трансдукционных сигнальных пути, вызываемые активацией глутаматных рецепторов N-метил-D-аспартата (НМДА). Первый путь – ионотропный, обусловлен открытием катионных каналов рецепторов при совпадении деполяризации постсинаптической мембраны, устраняющей магниевый блок катионных каналов, и пресинаптического высвобождения глутамата. В этих условиях в цитоплазму нейрона поступают Са2+, которые активируют Са-зависимые протеинкиназы (СаМКII, ПКА, ПКС, Src) или протеинфосфатазы (РР1, РР2В). Киназы и фосфатазы меняют либо плотность АМРА и НМДА глутаматных рецепторов в постсинаптических мембранах, либо меняют пресинаптическое высвобождение глутамата. Эти проявления синаптической пластичности лежат в основе разных форм долгосрочной памяти, обучения, накопления жизненного опыта. Второй, метаботропный сигнальный путь обусловлен движением внутриклеточных С-терминальных доменов субъединиц НМДА-рецепторов, их контактом и изменением активности киназ р38 и JNK2, которые вызывают снижение плотности АМРА глутаматных рецепторов в постсинаптических мембранах, элиминацию дендритных шипиков и увеличение спонтанного пресинаптического высвобождения глутамата. Усиление ионотропного сигнального пути НМДА глутаматных рецепторов лежит в основе большого и биполярного депрессивного расстройства, а также ишемических поражений мозга. Ослабление этого сигнального пути связывают с развитием шизофрении. Метаботропный трансдукционный путь НМДА-рецепторов вовлечен в развитие когнитивных и мнемотропных нарушений при болезни Альцгеймера.
Литература
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10. Dan Y, Poo MM Spike timing-dependent plasticity: from synapse to perception. Physiol Rev. 2006; 86 (3): 1033–1048. doi: 10.1152/physrev.00030.2005
11. Liu SJ, Zukin RS. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 2007; 30 (3): 126-134. doi: 10.1016/j.tins.2007.01.006
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14. Peng Y, Zhao J, Gu QH, et al. Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses. Hippocampus. 2010;20 (5):646–658. doi: 10.1002/hipo.20654
15. Watt AJ, Sjo¨stro¨m PJ, Ha¨usser M, et al. A proportionalbut slower NMDA potentiation follows AMPA potentiation in LTP. Nat Neurosci,2004;7 (5):518 –524. doi: 10.1038/nn1220
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17. Perin M, Longordo F, Massonnet C, et al. Diurnal inhibition of NMDA-EPSCs at rat hippocampal mossy fibre synapses through orexin-2 receptors. J Physiol. 2014; 592 (19):4277– 4295. doi: 10.1113/jphysiol.2014.272757
18. Morishita W, Marie H, Malenka RC. Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses. Nat Neurosci. 2005; 8 (8):1043–1050. doi: 10.1038/nn1506
19. Stanton PK. LTP, LTD, and the sliding of threshold for long-term synaptic plasticity. Hippocampus. 1996; 6 (1): 35-42. doi: 10.1002/(SICI)1098-1063(1996)6:1<35::AID-HIPO7>3.0.CO;2-6
20. Rebola N, Carta M, Mulle C. Operation and plasticity of hippocampal CA3 circuits: implications for memory encoding. Nat Rev Neurosci. 2017;18 (4):208 –220. doi: 10.1038/nrn.2017.10
21. Reese AL, Kavalali ET. Spontaneous neurotransmission signals through store-driven Ca2+ transients to maintain synaptic homeostasis. Elife. 2015; 4: doi: 10.7554/eLife.09262
22. Buchanan KA, Blackman AV, Moreau AW, et al. Target-specific expression of presynaptic NMDA receptors in neocortical microcircuits. Neuron. 2012;75 (3):451– 466. doi: 10.1016/j.neuron.2012.06.017
23. Dore K, Stein IS, Brock JA, et al. Unconventional NMDA receptor signaling, J Neurosci. 2017; 37 (45): 10800-10807. doi: 10.1523/JNEUROSCI.1825-17.2017
24. Larsen RS, Corlew RJ, Henson MA, et al. NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity. Nat Neurosci. 2011; 14 (3):338 –344. doi: 10.1038/nn.2750
25. Abrahamsson T, Chou YC, Li SY, et al. Differential regulation of evoked and spontaneous release by presynaptic NMDA receptors. Neuron. 2017;96 (4): 839-855. doi: 10.1016/j.neuron.2017.09.030
26. Nabavi S, Kessels HW, Alfonso S, et al. Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc Nat AcadSci U S A. 2013; 110 (10): 4027–4032. doi: 10.1073/pnas.1219454110
27. Kohr G, Jensen V, Koester HJ, et al. Intracellular domains of NMDA receptor subtypes are
determinants for long-term potentiation induction. J Neurosci. 2003;23 (34): 10791-10799. PMCID: PMC6740988
28. Ryan TJ, Kopanitsa MV, Indersmitten T, et al. Evolution of GluN2A/B cytoplasmic domains diversified vertebrate synaptic plasticity and behavior. Nat Neurosci. 2013; 16 (1): 25-32. doi: 10.1038/nn.3277
29. Dore K, Aow J, Malinow R. Agonist binding to the NMDA receptor drives movement of its cytoplasmic domain without ion flow. Proc NatAcadSci U S A. 2015; 112 (47):14705–14710. doi: 10.1073/pnas.1520023112
30. Nistico` R, Florenzano F, Mango D, et al. Presynaptic c-Jun N-terminal Kinase 2regulates NMDA receptor-dependent glutamate release. Sci Rep. 2015; 5:9035. doi: 10.1038/srep09035
31. Stein IS, Gray JA, Zito K. Non-ionotropic NMDA receptor signaling drives activity-induced dendritic spine shrinkage. J Neurosci. 2015; 35 (35): 12303–12308. doi: 10.1523/JNEUROSCI.4289-14.2015
32. Razoux F, Garcia R, Lrna I. Ketamine, at dose that disrupts motor behavior and latent inhibition, enhances prefrontal cortex synaptic efficacy and glutamate release in the nucleus accumbens. Neuropsychopharmacology. 2007; 32 (3): 719–727. doi: 10.1038/sj.npp.1301057
33. Li B, Devidze N, Barengolts D, et al. NMDA receptor phosphorilation at a site affected in schizophrenia controls synaptic and behavioral plasticity. J Neurosci. 2009; 29 (38): 11965–11972. doi: 10.1523/JNEUROSCI.2109-09.2009
34. Stephan KE, Friston KJ, Fritch CD. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bull. 2009; 35 (3): 509–527. doi: 10.1093/schbul/sbn176
35. Miyamoto Y, Yamada K, Noda Y, et al. Hyperfunction of dopaminergic and serotonergic neuronal systems in mice lacking the NMDA receptor epsilon1 subuni. J Neurosci. 2001;21(2): 750–757. PMCID: PMC6763826
36. Wang X, Zhong P, Gu Z, Yan Z. Regulation of NMDA receptors by dopamine D4 signaling in prefrontal cortex. J Neurosci. 2003; 23 (30): 9852–9861. PMCID: PMC6740894
37. Li Y-C, Xi D, Roman J, et al. Activation of glycogen synthase kinase-3β is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J Neurosci. 2009; 29 (49): 15551–15563. doi: 10.1523/JNEUROSCI.3336-09.2009
38. Rajkowska G, Miguel-Hidalgo JJ, Wei J, et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry. 1999; 45 (9): 1085–1098. doi: 10.1016/s0006-3223(99)00041-4
39. Sun P, Wang F, Wang L, et al. Increase in cortical pyramidal cell excitability accopanies depression-like behavior in mice: a transcranial magnetic stimulation study. J Neurosci. 2011; 31 (45): 16464–16472. doi: 10.1523/JNEUROSCI.1542-11.2011
40. Abramets II, Evdokimov DV, Talalayenko AN. Glutamatergic synaptic transmission in rat cerebral cortex mediated by ionotropic glutamate receptors under behavioral depression. Researches in Neurology: an International Journal. 2013.article ID 1591123. doi: 10.5171/2013.159123
41. Abramets II, Evdokimov DV, Zayka TO. The alterations of neurophysiological parameters of anterior cingulate cortex in the experimental depression syndrome of different genesis. IP Pavlov Rus Med Biol Herald. 2016; 24 (2): 22-30.
42. Przewlocki R, Parsons KL, Sweeney DS, et al. Enhancement of calcium oscillations and burst events involving NMDA receptors and calcium channels in cultured hippocampal neurons. J Neurosci. 1999; 19 (22): 9705–9715. PMCID: PMC6782974
43. Bagley J, Moghaddam B. Temporal dynamics of glutamate efflux in the prefrontal cortex and in hippocampus following repeated stress: effects of pretreatment with saline and diazepam. Neuroscience. 1997;77(1): 65–73. doi: 10.1016/s0306-4522(96)00435-6
44. Yang C-H, Huang C-C, Hsu K-S. Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J Neurosci. 2005;25(17): 4288–4293. doi: 10.1523/JNEUROSCI.0406-05.2005
45. Liu Y, Wong TP, Aarts M, et al. NMDA receptor subunits have differential roles in mediating exitotoxic neuronal death in vitro and in vivo. J Neurosci. 2007; 27 (11): 2846–2857. doi: 10.1523/JNEUROSCI.0116-07.2007
46. Shankar GM, Bloodgood BL, Townsend M, t al. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci. 2007; 27 (11):2866–28757. doi: 10.1523/JNEUROSCI.4970-06.2007
47. Kessels HW, Nabavi S, Malinow R. Metabotropic NMDA receptor function is required for beta-amyloid-induced synaptic depression. ProcNat AcadSci U S A. 2013;110 (10):4033– 4038. doi: 10.1073/pnas.1219605110
48. Al-Hallaq RA, Conrads TP, Veenstra TD, Wenthold RJ. NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J Neurosci. 2007; 27 (31): 8334-8343. doi: 10.1523/JNEUROSCI.2155-07.2007
49. Birnbaum JH, Bali J, Rajendran L, et al. Calcium flux-independent NMDA receptor activity is required for A beta oligomer-induced synaptic loss. Cell Death Dis. 2015; 6: e1791. doi: 10.1038/cddis.2015.160
2. Conn, P.J., Pin, J.P. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev PharmacolToxicol. 1997; 37: 205-237. doi: 10.1146/annurev.pharmtox.37.1.205
3. Traynelis, S.F., Wollmuth, L.P., McBain, C.J., et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev. 2010; 62 (3): 405-496. doi: 10.1124/pr.109.002451
4. Kotecha S.A,. MacDonald J.F. Signaling molecules and receptor transduction cascades that regulate NMDA receptor mediated synaptic transmission. Int Rev Neurobiol. 2003;54 (1): 51–106. doi: 10.1016/s0074-7742(03)54003-x
5. McBain CJ, Mayer ML. N-methyl-D-aspartic acid receptor structure and function. Physiol Rev. 1994; 74 (3):723–760. doi: 10.1152/physrev.1994.74.3.723
6. Iacobucci GJ, Popescu GK. NMDA receptors: linking physiological output to biophysical operation. Nat Rev Neurosci. 2017; 18 (4):236 –249. doi: 10.1038/nrn.2017.24
7. Lu¨scher C, Malenka RC. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring HarbPerspectBiol. 2012; Jun 1;4(6). pii: a005710. doi: 10.1101/cshperspect.a005710
8. Lee HK, Barbarosie M, Kameyama K, et al. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature. 2000; 405 (6789): 955-959. doi: 10.1038/35016089
9. Montgomery JM, Selcher JC, Hanson JE, Madison DV. Dynamin-dependent NMDAR endocytosis during LTD and its dependence on synaptic state. BMC Neurosci. 2005 Jul 22; 6: 48. doi: 10.1186/1471-2202-6-48
10. Dan Y, Poo MM Spike timing-dependent plasticity: from synapse to perception. Physiol Rev. 2006; 86 (3): 1033–1048. doi: 10.1152/physrev.00030.2005
11. Liu SJ, Zukin RS. Ca2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci. 2007; 30 (3): 126-134. doi: 10.1016/j.tins.2007.01.006
12. Harnett MT, Bernier BE, Ahn KC, Morikawa H. Burst-timing-dependent plasticity of NMDA receptor-mediated transmission in midbrain dopamine neurons. Neuron. 2009; 62 (6): 826-838. doi: 10.1016/j.neuron.2009.05.011
13. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron. 2004; 44 (1): 5-21. doi: 10.1016/j.neuron.2004.09.012
14. Peng Y, Zhao J, Gu QH, et al. Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses. Hippocampus. 2010;20 (5):646–658. doi: 10.1002/hipo.20654
15. Watt AJ, Sjo¨stro¨m PJ, Ha¨usser M, et al. A proportionalbut slower NMDA potentiation follows AMPA potentiation in LTP. Nat Neurosci,2004;7 (5):518 –524. doi: 10.1038/nn1220
16. Hunt DL, Puente N, Grandes P, Castillo PE Bidirectional NMDA receptor plasticity controls CA3 output and heterosynaptic metaplasticity. Nat Neurosci. 2013; 16 (8):1049 –1059. doi: 10.1038/nn.3461
17. Perin M, Longordo F, Massonnet C, et al. Diurnal inhibition of NMDA-EPSCs at rat hippocampal mossy fibre synapses through orexin-2 receptors. J Physiol. 2014; 592 (19):4277– 4295. doi: 10.1113/jphysiol.2014.272757
18. Morishita W, Marie H, Malenka RC. Distinct triggering and expression mechanisms underlie LTD of AMPA and NMDA synaptic responses. Nat Neurosci. 2005; 8 (8):1043–1050. doi: 10.1038/nn1506
19. Stanton PK. LTP, LTD, and the sliding of threshold for long-term synaptic plasticity. Hippocampus. 1996; 6 (1): 35-42. doi: 10.1002/(SICI)1098-1063(1996)6:1<35::AID-HIPO7>3.0.CO;2-6
20. Rebola N, Carta M, Mulle C. Operation and plasticity of hippocampal CA3 circuits: implications for memory encoding. Nat Rev Neurosci. 2017;18 (4):208 –220. doi: 10.1038/nrn.2017.10
21. Reese AL, Kavalali ET. Spontaneous neurotransmission signals through store-driven Ca2+ transients to maintain synaptic homeostasis. Elife. 2015; 4: doi: 10.7554/eLife.09262
22. Buchanan KA, Blackman AV, Moreau AW, et al. Target-specific expression of presynaptic NMDA receptors in neocortical microcircuits. Neuron. 2012;75 (3):451– 466. doi: 10.1016/j.neuron.2012.06.017
23. Dore K, Stein IS, Brock JA, et al. Unconventional NMDA receptor signaling, J Neurosci. 2017; 37 (45): 10800-10807. doi: 10.1523/JNEUROSCI.1825-17.2017
24. Larsen RS, Corlew RJ, Henson MA, et al. NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity. Nat Neurosci. 2011; 14 (3):338 –344. doi: 10.1038/nn.2750
25. Abrahamsson T, Chou YC, Li SY, et al. Differential regulation of evoked and spontaneous release by presynaptic NMDA receptors. Neuron. 2017;96 (4): 839-855. doi: 10.1016/j.neuron.2017.09.030
26. Nabavi S, Kessels HW, Alfonso S, et al. Metabotropic NMDA receptor function is required for NMDA receptor-dependent long-term depression. Proc Nat AcadSci U S A. 2013; 110 (10): 4027–4032. doi: 10.1073/pnas.1219454110
27. Kohr G, Jensen V, Koester HJ, et al. Intracellular domains of NMDA receptor subtypes are
determinants for long-term potentiation induction. J Neurosci. 2003;23 (34): 10791-10799. PMCID: PMC6740988
28. Ryan TJ, Kopanitsa MV, Indersmitten T, et al. Evolution of GluN2A/B cytoplasmic domains diversified vertebrate synaptic plasticity and behavior. Nat Neurosci. 2013; 16 (1): 25-32. doi: 10.1038/nn.3277
29. Dore K, Aow J, Malinow R. Agonist binding to the NMDA receptor drives movement of its cytoplasmic domain without ion flow. Proc NatAcadSci U S A. 2015; 112 (47):14705–14710. doi: 10.1073/pnas.1520023112
30. Nistico` R, Florenzano F, Mango D, et al. Presynaptic c-Jun N-terminal Kinase 2regulates NMDA receptor-dependent glutamate release. Sci Rep. 2015; 5:9035. doi: 10.1038/srep09035
31. Stein IS, Gray JA, Zito K. Non-ionotropic NMDA receptor signaling drives activity-induced dendritic spine shrinkage. J Neurosci. 2015; 35 (35): 12303–12308. doi: 10.1523/JNEUROSCI.4289-14.2015
32. Razoux F, Garcia R, Lrna I. Ketamine, at dose that disrupts motor behavior and latent inhibition, enhances prefrontal cortex synaptic efficacy and glutamate release in the nucleus accumbens. Neuropsychopharmacology. 2007; 32 (3): 719–727. doi: 10.1038/sj.npp.1301057
33. Li B, Devidze N, Barengolts D, et al. NMDA receptor phosphorilation at a site affected in schizophrenia controls synaptic and behavioral plasticity. J Neurosci. 2009; 29 (38): 11965–11972. doi: 10.1523/JNEUROSCI.2109-09.2009
34. Stephan KE, Friston KJ, Fritch CD. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bull. 2009; 35 (3): 509–527. doi: 10.1093/schbul/sbn176
35. Miyamoto Y, Yamada K, Noda Y, et al. Hyperfunction of dopaminergic and serotonergic neuronal systems in mice lacking the NMDA receptor epsilon1 subuni. J Neurosci. 2001;21(2): 750–757. PMCID: PMC6763826
36. Wang X, Zhong P, Gu Z, Yan Z. Regulation of NMDA receptors by dopamine D4 signaling in prefrontal cortex. J Neurosci. 2003; 23 (30): 9852–9861. PMCID: PMC6740894
37. Li Y-C, Xi D, Roman J, et al. Activation of glycogen synthase kinase-3β is required for hyperdopamine and D2 receptor-mediated inhibition of synaptic NMDA receptor function in the rat prefrontal cortex. J Neurosci. 2009; 29 (49): 15551–15563. doi: 10.1523/JNEUROSCI.3336-09.2009
38. Rajkowska G, Miguel-Hidalgo JJ, Wei J, et al. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry. 1999; 45 (9): 1085–1098. doi: 10.1016/s0006-3223(99)00041-4
39. Sun P, Wang F, Wang L, et al. Increase in cortical pyramidal cell excitability accopanies depression-like behavior in mice: a transcranial magnetic stimulation study. J Neurosci. 2011; 31 (45): 16464–16472. doi: 10.1523/JNEUROSCI.1542-11.2011
40. Abramets II, Evdokimov DV, Talalayenko AN. Glutamatergic synaptic transmission in rat cerebral cortex mediated by ionotropic glutamate receptors under behavioral depression. Researches in Neurology: an International Journal. 2013.article ID 1591123. doi: 10.5171/2013.159123
41. Abramets II, Evdokimov DV, Zayka TO. The alterations of neurophysiological parameters of anterior cingulate cortex in the experimental depression syndrome of different genesis. IP Pavlov Rus Med Biol Herald. 2016; 24 (2): 22-30.
42. Przewlocki R, Parsons KL, Sweeney DS, et al. Enhancement of calcium oscillations and burst events involving NMDA receptors and calcium channels in cultured hippocampal neurons. J Neurosci. 1999; 19 (22): 9705–9715. PMCID: PMC6782974
43. Bagley J, Moghaddam B. Temporal dynamics of glutamate efflux in the prefrontal cortex and in hippocampus following repeated stress: effects of pretreatment with saline and diazepam. Neuroscience. 1997;77(1): 65–73. doi: 10.1016/s0306-4522(96)00435-6
44. Yang C-H, Huang C-C, Hsu K-S. Behavioral stress enhances hippocampal CA1 long-term depression through the blockade of the glutamate uptake. J Neurosci. 2005;25(17): 4288–4293. doi: 10.1523/JNEUROSCI.0406-05.2005
45. Liu Y, Wong TP, Aarts M, et al. NMDA receptor subunits have differential roles in mediating exitotoxic neuronal death in vitro and in vivo. J Neurosci. 2007; 27 (11): 2846–2857. doi: 10.1523/JNEUROSCI.0116-07.2007
46. Shankar GM, Bloodgood BL, Townsend M, t al. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci. 2007; 27 (11):2866–28757. doi: 10.1523/JNEUROSCI.4970-06.2007
47. Kessels HW, Nabavi S, Malinow R. Metabotropic NMDA receptor function is required for beta-amyloid-induced synaptic depression. ProcNat AcadSci U S A. 2013;110 (10):4033– 4038. doi: 10.1073/pnas.1219605110
48. Al-Hallaq RA, Conrads TP, Veenstra TD, Wenthold RJ. NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J Neurosci. 2007; 27 (31): 8334-8343. doi: 10.1523/JNEUROSCI.2155-07.2007
49. Birnbaum JH, Bali J, Rajendran L, et al. Calcium flux-independent NMDA receptor activity is required for A beta oligomer-induced synaptic loss. Cell Death Dis. 2015; 6: e1791. doi: 10.1038/cddis.2015.160
Опубликована
2020-06-01
Как цитировать
ЕВДОКИМОВ, Д. В.; КУЗНЕЦОВ, Ю. В.; СИДОРОВА, Ю. В..
ДВОЙСТВЕННЫЕ ТРАНСДУКЦИОННЫЕ ФУНКЦИИ НЕЙРОНАЛЬНЫХ ГЛУТАМАТНЫХ РЕЦЕПТОРОВ N-МЕТИЛ-D-АСПАРТАТА И ИХ РОЛЬ В ФИЗИОЛОГИИ И ПАТОЛОГИИ ГОЛОВНОГО МОЗГА.
Университетская клиника, [S.l.], n. 2(35), p. 67-77, июнь 2020.
ISSN 1819-0464. Доступно на: <http://journal.dnmu.ru/index.php/UC/article/view/497>. Дата доступа: 01 май 2024
doi: https://doi.org/10.26435/uc.v0i2(35).497.
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