Ключевые слова
кортикостерон
стресс
гиппокамп
префронтальная кора
амигдала
минералокортикоидный рецептор
глюкокортикоидный рецептор
AMPA-рецептор
NMDA-рецептор
Как цитировать
Аннотация
Глюкокортикоиды, высвобождающиеся из коры надпочечников при действии стрессорных факторов, являются важнейшими медиаторами интегративной регуляции адаптивной пластичности мозга, осуществляемой нейрогуморальной гипоталамо-гипофизарно-надпочечниковой системой. Возбуждающие синапсы рассматриваются как ключевые участники синаптической пластичности и поведенческой адаптации. В обзоре представлены накопленные к настоящему времени данные о механизмах глюкокортикоидной регуляции глутаматергического синапса, в первую очередь, на примерах гиппокампа и префронтальной коры. Глюкокортикоиды, запуская трансдукцию сигнала через минералокортикоидные и глюкокортикоидные рецепторы, локализованные на синаптических мембранах и в цитозоле глутаматергических нейронов, регулируют пластичность синапса на уровне пре- и постсинаптического компартментов. Глюкокортикоиды модулируют возбудимость синапса за счет изменений везикулярного транспорта и высвобождения глутамата, опосредуют изменения экспрессии, состава и свойств ионотропных NMDA- и AMPA- и других глутаматных рецепторов. Представлена подробная схема множественных регуляторных механизмов, реализуемых в глутаматергическом синапсе при связывании глюкокортикоидов со специфическими рецепторами.
Литература
Gulyaeva NV (2019) Biochemical Mechanisms and Translational Relevance of Hippocampal Vulnerability to Distant Focal Brain Injury: The Price of Stress Response. Biochemistry (Mosc) 84(11):1306-1328. https://doi.org/10.1134/S0006297919110087
de Kloet ER, Meijer OC, de Nicola AF, de Rijk RH, Joëls M (2018) Importance of the brain corticosteroid receptor balance in metaplasticity,cognitive performance and neuro-inflammation. Front Neuroendocrinol 49:124-145. https://doi.org/10.1016/j.yfrne.2018.02.003
Prager EM, Johnson LR (2009) Stress at the synapse: signal transduction mechanisms of adrenal steroids at neuronal membranes. Sci Signal 2(86):re5. https://doi.org/ 10.1126/scisignal.286re5
Gulyaeva NV (2017) Molecular Mechanisms of Neuroplasticity: An Expanding Universe. Biochemistry (Mosc) 82:237-242. https://doi.org/ 10.1134/S0006297917030014
Xiong H, Krugers HJ (2015) Tuning hippocampal synapses by stress-hormones: Relevance for emotional memory formation. Brain Res 1621:114-120. https://doi.org/ 10.1016/j.brainres.2015.04.010
Gulyaeva N (2019) Functional Neurochemistry of the Ventral and Dorsal Hippocampus:Stress, Depression, Dementia and Remote Hippocampal Damage. Neurochem Res 44:1306-1322. https://doi.org/ 10.1007/s11064-018-2662-0
Podgorny OV, Gulyaeva NV (2020) Glucocorticoid-mediated mechanisms of hippocampal damage: Contribution of subgranular neurogenesis. J Neurochem. https://doi.org/10.1111/jnc.15265
Kessels HW, Malinow R (2009) Synaptic AMPA receptor plasticity and behaviour. Neuron 61:340–350. https://doi.org/ 10.1016/j.neuron.2009.01.015
Timmermans W, Xiong H, Hoogenraad CC, Krugers HJ (2013) Stress and excitatory synapses: from health to disease. Neuroscience 248:626-636. https://doi.org/ 10.1016/j.neuroscience.2013.05.043
Gulyaeva NV (2020) Hippocampal hyperglutamatergic signaling matters: Early targeting glutamate neurotransmission as a preventive strategy in Alzheimer's disease: An Editorial Highlight for "Riluzole attenuates glutamatergic tone and cognitive decline in AβPP/PS1 mice" J Neurochem. https://doi.org/: 10.1111/jnc.15238
Halpain S, McEwen BS (1988) Corticosterone decreases 3H-glutamate binding in rat hippocampal formation. Neuroendocrinology 48:235-241. https://doi.org/ 10.1159/000125017
Armanini MP, Hutchins C, Stein BA, Sapolsky RM (1990) Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res 532:7-12. https://doi.org/10.1016/0006-8993(90)91734-x
Virgin CE Jr, Ha TP, Packan DR, Tombaugh GC, Yang SH, Horner HC, Sapolsky RM (1991) Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J Neurochem 57:1422-1428. https://doi.org/10.1111/j.1471-4159.1991.tb08309.x
Sandi C (1998) The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast 6:41-52. https://doi.org/ 10.1155/NP.1998.41
Karst H, Joëls M (2003) Effect of chronic stress on synaptic currents in rat hippocampal dentate gyrus neurons. J Neurophysiol 89:625-633. https://doi.org/ 10.1152/jn.00691.2002
Kvarta MD, Bradbrook KE, Dantrassy HM, Bailey AM, Thompson SM (2015) Corticosterone mediates the synaptic and behavioral effects of chronic stress at rat hippocampal temporoammonic synapses. J Neurophysiol 114:1713-1724. https://doi.org/ 10.1152/jn.00359.2015
Martin S, Henley J, Holman D, Zhou M, Wiegert O, van Spronsen M, Joëls M, Hoogenraad CC, Krugers HJ (2009) Corticosterone alters AMPAR mobility and facilitates bidirectional synaptic plasticity. PLoS One. 4(3):e4714. https://doi.org/ 10.1371/journal.pone.0004714
Groc L, Choquet D, Chaouloff F (2008) The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 11:868-870. https://doi.org/10.1038/nn.2150
Conboy L, Sandi C (2010) Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action. Neuropsychopharmacology 35(3):674-685. https://doi.org/10.1038/npp.2009.172
Choi GE, Oh JY, Lee HJ, Chae CW, Kim JS, Jung YH, Han HJ (2018) Glucocorticoid-mediated ER-mitochondria contacts reduce AMPA receptor and mitochondria trafficking into cell terminus via microtubule destabilization. Cell Death Dis 9:1137. https://doi.org/ 10.1038/s41419-018-1172-y
Tse YC, Bagot RC, Wong TP (2012) Dynamic regulation of NMDAR function in the adult brain by the stress hormone corticosterone. Front Cell Neurosci 6:9. https://doi.org/ 10.3389/fncel.2012.00009
Mikasova L, Xiong H, Kerkhofs A, Bouchet D, Krugers HJ, Groc L (2017) Stress hormone rapidly tunes synaptic NMDA receptor through membrane dynamics and mineralocorticoid signalling. Sci Rep 7:8053. https://doi.org/ 10.1038/s41598-017-08695-3
Tse YC, Bagot RC, Hutter JA, Wong AS, Wong TP (2011) Modulation of synaptic plasticity by stress hormone associates with plastic alteration of synaptic NMDA receptor in the adult hippocampus. PLoS One 6:e27215. https://doi.org/ 10.1371/journal.pone.0027215
Krugers HJ, Alfarez DN, Karst H, Parashkouhi K, van Gemert N, Joëls M (2005) Corticosterone shifts different forms of synaptic potentiation in opposite directions. Hippocampus 15:697-703. https://doi.org/ 10.1002/hipo.20092
Zhang Y, Sheng H, Qi J, Ma B, Sun J, Li S, Ni X (2012) Glucocorticoid acts on a putative G protein-coupled receptor to rapidly regulate the activity of NMDA receptors in hippocampal neurons. Am J Physiol Endocrinol Metab 302:E747-E58. https://doi.org/10.1152/ajpendo.00302.2011
Komatsuzaki Y, Hatanaka Y, Murakami G, Mukai H, Hojo Y, Saito M, Kimoto T, Kawato S (2012) Corticosterone induces rapid spinogenesis via synaptic glucocorticoid receptors and kinase networks in hippocampus. PLoS One: 7e34124. https://doi.org/ 10.1371/journal.pone.0034124
Chaouloff F, Hémar A, Manzoni O (2008) Local facilitation of hippocampal metabotropic glutamate receptor-dependent long-term depression by corticosteroneand dexamethasone. Psychoneuroendocrinology 33:686-691. https://doi.org/ 10.1016/j.psyneuen.2007.12.013
Hunter RG, Bellani R, Bloss E, Costa A, McCarthy K, McEwen BS (2009) Regulation of kainate receptor subunit mRNA by stress and corticosteroids in the rat hippocampus. PLoS One 4:e4328. https://doi.org/ 10.1371/journal.pone.0004328
McCauley JP, Petroccione MA, D'Brant LY, Todd GC, Affinnih N, Wisnoski JJ, Zahid S, Shree S, Sousa AA, De Guzman RM, Migliore R, Brazhe A, Leapman RD, Khmaladze A, Semyanov A, Zuloaga DG, Migliore M, Scimemi A (2020) Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1. Cell Rep 33:108255. https://doi.org/ 10.1016/j.celrep.2020.108255
Sarabdjitsingh RA, Jezequel J, Pasricha N, Mikasova L, Kerkhofs A, Karst H, Groc L, Joëls M (2014) Ultradian corticosterone pulses balance glutamatergictransmission and synaptic plasticity. Proc Natl Acad Sci U S A 111:14265-14270. https://doi.org/ 10.1073/pnas.1411216111
Sarabdjitsingh RA, Pasricha N, Smeets JA, Kerkhofs A, Mikasova L, Karst H, Groc L, Joëls M (2016) Hippocampal Fast Glutamatergic Transmission Is Transiently Regulated by Corticosterone Pulsatility. PLoS One 11:e0145858. https://doi.org/ 10.1371/journal.pone.0145858
Yuen EY, Wei J, Yan Z (2017) Molecular and Epigenetic Mechanisms for the Complex Effects of Stress on Synaptic Physiology and Cognitive Functions. Int J Neuropsychopharmacol 20(11):948-955. https://doi.org/10.1093/ijnp/pyx052
Musazzi L, Treccani G, Popoli M (2015) Functional and structural remodeling of glutamate synapses in prefrontal and frontal cortex induced by behavioral stress. Front Psychiatry 6:60. https://doi.org/ 10.3389/fpsyt.2015.00060
Bonini D, Mora C, Tornese P, Sala N, Filippini A, La Via L, Milanese M, Calza S, Bonanno G, Racagni G, Gennarelli M, Popoli M, Musazzi L, Barbon A (2016) Acute Footshock Stress Induces Time-Dependent Modifications of AMPA/NMDA Protein Expression and AMPA Phosphorylation. Neural Plast 2016:7267865. https://doi.org/ 10.1155/2016/7267865
Nava N, Treccani G, Liebenberg N, Chen F, Popoli M, Wegener G, Nyengaard JR (2014) Chronic desipramine prevents acute stress-induced reorganization of medial prefrontal cortex architecture by blocking glutamate vesicle accumulation and excitatory synapse increase. Int J Neuropsychopharmacol 18:pyu085. https://doi.org/ 10.1093/ijnp/pyu085
Musazzi L, Tornese P, Sala N, Popoli M (2017) Acute stress is not acute: sustained enhancement of glutamate release after acute stress involves readily releasable pool size and synapsin I activation. Mol Psychiatry 22:1226-1227. https://doi.org/10.1038/mp.2016.175
Toya S, Takatsuru Y, Kokubo M. Amano I, Shimokawa N, Koibuchi N (2014) Early-life-stress affects the homeostasis of glutamatergic synapses. Eur J Neurosci 40:3627-3634. https://doi.org/10.1111/ejn.12728
Karst H, Berger S, Erdmann G, Schütz G, Joëls M (2010) Metaplasticity of amygdalar responses to the stress hormone corticosterone. Proc Natl Acad Sci U S A 107:14449-14454. https://doi.org/ 10.1073/pnas.0914381107
Hartmann J, Dedic N, Pöhlmann ML, Häusl A, Karst H, Engelhardt C, Westerholz S, Wagner KV, Labermaier C, Hoeijmakers L, Kertokarijo M, Chen , Joëls M, Deussing JM, Schmidt MV (2017) Forebrain glutamatergic, but not GABAergic, neurons mediate anxiogenic effects of the glucocorticoid receptor. Mol Psychiatry 22:466-475. https://doi.org/ 10.1038/mp.2016.87
Zhou JJ, Gao Y, Zhang X, Kosten TA, Li DP (2018) Enhanced Hypothalamic NMDA Receptor Activity Contributes to Hyperactivity of HPA Axis in Chronic Stress in Male Rats. Endocrinology 159:1537-1546. https://doi.org/10.1210/en.2017-03176
Caudal D, Rame M, Jay TM, Godsil BP (2016) Dynamic Regulation of AMPAR Phosphorylation In Vivo Following Acute Behavioral Stress. Cell Mol Neurobiol 36:1331-1342. https://doi.org/ 10.1007/s10571-016-0332-9
Caudal D, Godsil BP, Mailliet F, Bergerot D, Jay TM (2010) Acute stress induces contrasting changes in AMPA receptor subunit phosphorylation within the prefrontal cortex, amygdala and hippocampus PLoS One. 5:e15282. https://doi.org/ 10.1371/journal.pone.0015282
Pillai AG, Arp M, Velzing E, Lesuis SL, Schmidt MV, Holsboer F, Joëls M, Krugers HJ. (2018) Early life stress determines the effects of glucocorticoids and stress on hippocampal function: Electrophysiological and behavioral evidence respectively. Neuropharmacology 133:307-318. https://doi.org/ 10.1016/j.neuropharm.2018.02.001
Gulyaeva NV (2017) Interplay between Brain BDNF and Glutamatergic Systems: A Brief State of the Evidence and Association with the Pathogenesis of Depression. Biochemistry (Mosc) 82:301-307. https://doi.org/ 10.1016/j.ejphar.2013.07.015
Joëls M, Pasricha N, Karst H (2013) The interplay between rapid and slow corticosteroid actions in brain. Eur J Pharmacol 719:44-52. https://doi.org/
Joëls M, de Kloet ER (2017) 30 Years of the mineralocorticoid receptor: The brain mineralocorticoid receptor: a saga in three episodes. J Endocrinol 234:T49-T66. https://doi.org/ 10.1530/JOE-16-0660
Le Menuet D, Lombès M (2014).The neuronal mineralocorticoid receptor: from cell survival to neurogenesis. Steroids 91:11-19. https://doi.org/ 10.3389/fendo.2016.00066
Suri D, Vaidya VA (2013).Glucocorticoid regulation of brain-derived neurotrophic factor: relevance to hippocampal structural and functional plasticity. Neuroscience 239:196-213.
Гуляева НВ (2020) Физиологический континуум пластичности и патологии нервной системы. Интегративная физиология 1: 294–302. [Gulyaeva NV (2020) Physiological continuum of plasticity and pathology of the nervous system. Integrative Physiol 1:294–302. (In Russ)]. https://doi.org/10.33910/2687-1270-2020-1-4-294-302