ОСОБЕННОСТИ ПУРИНЕРГИЧЕСКОЙ МОДУЛЯЦИИ В ГИППОКАМПЕ НОВОРОЖДЕННЫХ КРЫС
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Ключевые слова

аденозин
АТФ
гигантский деполяризующий потенциал
нейрон
пуринорецептор
гиппокамп

Аннотация

Уже в раннем постнатальном периоде в различных отделах нервной системы, включая гиппокамп, наблюдается ритмическая электрическая активность. В гиппокампе этот феномен проявляется в виде гигантских деполяризующих потенциалов (ГДП), которые играют ключевую роль в росте нейронов и формировании межнейронных связей. Генерация и распространение ГДП регулируются множеством механизмов, среди которых особое место занимает пуринергическая система (с участием АТФ и аденозина), изученная нами. Наши исследования показали, что во время ГДП происходит выделение АТФ во внеклеточное пространство с последующим его гидролизом до аденозина. АТФ и аденозин способны модулировать активность как нейронов, так и глиальных клеток новорожденных через различные типы пуринергических рецепторов. В данном обзоре систематизированы современные данные о разнообразии эффектов пуринергической модуляции в гиппокампе новорожденных, феномене разнонаправленного действия пуринергических сигналов, экспрессии и функциональной роли всех подтипов пуринорецепторов в постнатальном периоде. Особое внимание уделено физиологической роли пуринергической модуляции в развивающемся гиппокампе.

https://doi.org/10.31857/S0044452925020024
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Литература

Luo L (2021) Architectures of neuronal circuits. Science 373(6559): eabg7285. s://doi.org/10.1126/science.abg7285

Bressan C, Saghatelyan A (2021) Intrinsic mechanisms regulating neuronal migration in the postnatal brain. Front Cell Neurosci 14: 620379. s://doi.org/10.3389/fncel.2020.620379

Warm D, Schroer J, Sinning A (2022) Gabaergic interneurons in early brain development: conducting and orchestrated by cortical network activity. Front Mol Neurosci 14: 807969. s://doi.org/10.3389/fnmol.2021.807969

Klavinskis-Whiting S, Bitzenhofer S, Hanganu-Opatz I, Ellender T (2023) Generation and propagation of bursts of activity in the developing basal ganglia. Cereb Cortex 33(20): 10595–10613. s://doi.org/10.1093/cercor/bhad307

Shevtsova NA, Ha NT, Rybak IA, Dougherty KJ (2020) Neural interactions in developing rhythmogenic spinal networks: insights from computational modeling. Front Neural Circuits 14: 614615. s://doi.org/10.3389/fncir.2020.614615

Zhang Z, Collins DC, Maier JX (2021) Network dynamics in the developing piriform cortex of unanesthetized rats. Cereb Cortex 31(2): 1334–1346. s://doi.org/10.1093/cercor/bhaa300

Riyahi P, Phillips MA, Colonnese MT (2021) Input-independent homeostasis of developing thalamocortical activity. eNeuro 8(3): ENEURO.0184-21.2021. s://doi.org/10.1523/ENEURO.0184-21.2021

Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol 416: 303–325. s://doi.org/10.1113/jphysiol.1989.sp017762

Juzekaeva E, Nasretdinov A, Mukhtarov M, Shipkov D, Valeeva G, Khazipov R (2024) Comparison of extracellular giant depolarizing potentials in vitro and early sharp waves in vivo in the CA1 hippocampus of neonatal rats. Biochem Biophys Res Commun 735: 150823. s://doi.org/10.1016/j.bbrc.2024.150823

Murata Y, Colonnese MT (2020) GABAergic interneurons excite neonatal hippocampus in vivo. Sci Adv 6(24): eaba1430. s://doi.org/10.1126/sciadv.aba1430

Bocchio M, Gouny C, Angulo-Garcia D, Toulat T, Tressard T, Quiroli E, Baude A, Cossart R (2020) Hippocampal hub neurons maintain distinct connectivity throughout their lifetime. Nat Commun 11(1): 4559. s://doi.org/10.1038/s41467-020-18432-6

Ojanen S, Kuznetsova T, Kharybina Z, Voikar V, Lauri SE, Taira T (2023) Interneuronal GluK1 kainate receptors control maturation of GABAergic transmission and network synchrony in the hippocampus. Mol Brain 16(1): 43. s://doi.org/10.1186/s13041-023-01035-9

Bolea S, Avignone E, Berretta N, Sanchez-Andres JV, Cherubini E (1999) Glutamate controls the induction of GABA-mediated giant depolarizing potentials through AMPA receptors in neonatal hippocampal slices. J Neurophysiol 81(5): 2095–2102. s://doi.org/10.1152/jn.1999.81.5.2095

Márquez LA, Griego E, López Rubalcava C, Galván EJ (2023) NMDA receptor activity during postnatal development determines intrinsic excitability and mossy fiber long-term potentiation of CA3 pyramidal cells. Hippocampus 33(8): 906–921. s://doi.org/10.1002/hipo.23524

Khazipov R, Jensen FE (2022) Neurons and circuits during brain development. Neurobiology of the Epilepsies: From Epilepsy: A Comprehensive Textbook.

Sebastian ER, Quintanilla JP, Sánchez-Aguilera A, Esparza J, Cid E, de la Prida LM (2023) Topological analysis of sharp-wave ripple waveforms reveals input mechanisms behind feature variations. Nat Neurosci 26(12): 2171–2181. s://doi.org/10.1038/s41593-023-01471-9

Schieferstein N, Del Toro A, Evangelista R, Imbrosci B, Swaminathan A, Schmitz D, Maier N, Kempter R (2024) Propagation of sharp wave-ripple activity in the mouse hippocampal CA3 subfield in vitro. J Physiol 602(19): 5039–5059. s://doi.org/10.1113/JP285671

Kis N, Lükő B, Herédi J, Magó Á, Erlinghagen B, Ahmadi M, Raus Balind S, Irás M, Ujfalussy BB, Makara JK (2024) Cholinergic regulation of dendritic Ca2+ spikes controls firing mode of hippocampal CA3 pyramidal neurons. Proc Natl Acad Sci U S A 121(46): e2321501121. s://doi.org/10.1073/pnas.2321501121

Phelan KD, Shwe UT, Wu H, Zheng F (2024) Investigating contributions of canonical transient receptor potential channel 3 to hippocampal hyperexcitability and seizure-induced neuronal cell death. Int J Mol Sci 25(11): 6260. s://doi.org/10.3390/ijms25116260

Schoenfeld G, Carta S, Rupprecht P, Ayaz A, Helmchen F (2021) In vivo calcium imaging of CA3 pyramidal neuron populations in adult mouse hippocampus. eNeuro 8(4): ENEURO.0023-21.2021. s://doi.org/10.1523/ENEURO.0023-21.2021

Pires J, Nelissen R, Mansvelder HD, Meredith RM (2021) Spontaneous synchronous network activity in the neonatal development of mPFC in mice. Dev Neurobiol 81(2): 207–225. s://doi.org/10.1002/dneu.22811

Sipilä ST, Huttu K, Voipio J, Kaila K (2006) Intrinsic bursting of immature CA3 pyramidal neurons and consequent giant depolarizing potentials are driven by a persistent Na+ current and terminated by a slow Ca2+-activated K+ current. Eur J Neurosci 23(9): 2330–2338. s://doi.org/10.1111/j.1460-9568.2006.04757.x

Cellot G, Di Mauro G, Ricci C, Tiribelli C, Bellarosa C, Ballerini L (2025) Bilirubin triggers calcium elevations and dysregulates giant depolarizing potentials during rat hippocampus maturation. Cells 14(3): 172. s://doi.org/10.3390/cells14030172

Kasyanov AM, Safiulina VF, Voronin LL, Cherubini E (2004) GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A 101(11): 3967–3972. s://doi.org/10.1073/pnas.0305974101

Wu MW, Kourdougli N, Portera-Cailliau C (2024) Network state transitions during cortical development. Nat Rev Neurosci 25(8): 535–552. https://doi.org/10.1038/s41583-024-00824-y

Curtis DR, Duggan AW, Felix D, Johnston GA (1970) GABA, bicuculline and central inhibition. Nature 226(5252): 1222–1224. s://doi.org/10.1038/2261222a0

Cossart R, Khazipov R (2022) How development sculpts hippocampal circuits and function. Physiol Rev 102(1): 343–378. s://doi.org/10.1152/physrev.00044.2020

Allene C, Picardo MA, Becq H, Miyoshi G, Fishell G, Cossart R (2012) Dynamic changes in interneuron morphophysiological properties mark the maturation of hippocampal network activity. J Neurosci 32(19): 6688–6698. s://doi.org/10.1523/JNEUROSCI.0081-12.2012

Flossmann T, Kaas T, Rahmati V, Kiebel SJ, Witte OW, Holthoff K, Kirmse K (2019) Somatostatin interneurons promote neuronal synchrony in the neonatal hippocampus. Cell Rep 26(12): 3173–3182.e5. s://doi.org/10.1016/j.celrep.2019.02.061

Mòdol L, Moissidis M, Selten M, Oozeer F, Marín O (2024) Somatostatin interneurons control the timing of developmental desynchronization in cortical networks. Neuron 112(12): 2015–2030.e5. s://doi.org/10.1016/j.neuron.2024.03.014

Kasiyanov A, Fujii N, Tamamura H, Xiong H (2008) Modulation of network-driven, GABA-mediated giant depolarizing potentials by SDF-1α in the developing hippocampus. Developmental Neuroscience 30(4): 285–292. s://doi.org/10.1159/000112520

Pál B (2024) On the functions of astrocyte-mediated neuronal slow inward currents. Neural Regen Res 19(12): 2602–2612. s://doi.org/10.4103/NRR.NRR-D-23-01723

Robert V, Butola T, Basu J (2023) Cortical and thalamic inputs drive distinct hippocampal microcircuits to modulate synchronized activity during development. Neuron 111(6): 761–763. s://doi.org/10.1016/j.neuron.2023.02.031

Safiulina VF, Zacchi P, Taglialatela M, Yaari Y, Cherubini E (2008) Low expression of Kv7/M channels facilitates intrinsic and network bursting in the developing rat hippocampus. J Physiol 586(22): 5437–5453. s://doi.org/10.1113/jphysiol.2008.156257

Le Magueresse C, Safiulina V, Changeux JP, Cherubini E (2006) Nicotinic modulation of network and synaptic transmission in the immature hippocampus investigated with genetically modified mice. J Physiol 576(Pt 2): 533–546. s://doi.org/10.1113/jphysiol.2006.117572

Cellot G, Di Mauro G, Ricci C, Tiribelli C, Bellarosa C, Ballerini L (2025) Bilirubin Triggers Calcium Elevations and Dysregulates Giant Depolarizing Potentials During Rat Hippocampus Maturation. Cells 14(3): 172. s://doi.org/10.3390/cells14030172

Yang D, Qi G, Ort J, Witzig V, Bak A, Delev D, Koch H, Feldmeyer D (2024) Modulation of large rhythmic depolarizations in human large basket cells by norepinephrine and acetylcholine. Commun Biol 7(1): 885. s://doi.org/10.1038/s42003-024-06546-2

Pinna S, Kunz C, Halpern A, Harrison S A, Jordan S F, Ward J, Werner F, Lane N (2022) A prebiotic basis for ATP as the universal energy currency. PLoS Biol 20(10): e3001437. s://doi.org/10.1371/journal.pbio.3001437

Drury A N, Szent-Györgyi A (1929) The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J Physiol 68(3): 213–237. s://doi.org/10.1113/jphysiol.1929.sp002608

Dale H (1935) Pharmacology and nerve-endings (Walter Ernest Dixon Memorial Lecture). Proc R Soc Med 28(3): 319–332.

Westfall D P, Dalziel H H, Forsyth K M (2024) ATP as a neurotransmitter, cotransmitter, and neuromodulator. In: Adenosine and adenine nucleotides as regulators of cellular function, CRC Press. pp. 295–305.

Kennedy C (2021) ATP as a cotransmitter in sympathetic and parasympathetic nerves – another Burnstock legacy. Auton Neurosci 235: 102860. s://doi.org/10.1016/j.autneu.2021.102860

Kennedy C (2021) The P2Y/P2X divide: how it began. Biochem Pharmacol 187: 114408. s://doi.org/10.1016/j.bcp.2021.114408

Schrader J (2022) Ectonucleotidases as bridge between the ATP and adenosine world: reflections on Geoffrey Burnstock. Purinergic Signal 18(2): 193–198. s://doi.org/10.1007/s11302-022-09862-6

Di Virgilio F, Vultaggio-Poma V, Falzoni S, Giuliani A L (2023) Extracellular ATP: a powerful inflammatory mediator in the central nervous system. Neuropharmacology 224: 109333. s://doi.org/10.1016/j.neuropharm.2022.109333

Cho S H, Tóth K, Kim D, Vo P H, Lin C H, Handakumbura P P, Ubach A R, Evans S, Paša-Tolić L, Stacey G (2022) Activation of the plant mevalonate pathway by extracellular ATP. Nat Commun 13(1): 450. s://doi.org/10.1038/s41467-022-28150-w

Huang Z, Xie N, Illes P, Di Virgilio F, Ulrich H, Semyanov A, Verkhratsky A, Sperlagh B, Yu S G, Huang C, Tang Y (2021) From purines to purinergic signalling: molecular functions and human diseases. Signal Transduct Target Ther 6(1): 162. s://doi.org/10.1038/s41392-021-00553-z

Glaser T, Ulrich H (2023) Purinergic signaling in brain physiology. In: Purinergic Signaling in Neurodevelopment, Neuroinflammation and Neurodegeneration. Cham: Springer. pp. 23–40.

Sattler C, Benndorf K (2022) Enlightening activation gating in P2X receptors. Purinergic Signal 18(2): 177–191. s://doi.org/10.1007/s11302-022-09850-w

Wildner F, Neuhäusel T S, Klemz A, Kovács R, Ulmann L, Geiger J R P, Gerevich Z (2024) Extracellular ATP inhibits excitatory synaptic input on parvalbumin-positive interneurons and attenuates gamma oscillations via P2X4 receptors. Br J Pharmacol 181(11): 1635–1653. s://doi.org/10.1111/bph.16298

North RA (2016) P2X receptors. Philos Trans R Soc Lond B Biol Sci 371(1700): 20150427. s://doi.org/10.1098/rstb.2015.0427

Bennetts FM, Mobbs JI, Ventura S, Thal DM (2022) The P2X1 receptor as a therapeutic target. Purinergic Signal 18(4): 421–433. s://doi.org/10.1007/s11302-022-09880-4

Sivcev S, Kudova E, Zemkova H (2023) Neurosteroids as positive and negative allosteric modulators of ligand-gated ion channels: P2X receptor perspective. Neuropharmacology 234: 109542. s://doi.org/10.1016/j.neuropharm.2023.109542

Khakh BS, North R A (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442(7102): 527–532. s://doi.org/10.1038/nature04886

Sheng D, Hattori M (2022) Recent progress in the structural biology of P2X receptors. Proteins 90(10): 1779–1785. s://doi.org/10.1002/prot.26302

von Kügelgen I (2024) Pharmacological characterization of P2Y receptor subtypes – an update. Purinergic Signal 20(2): 99–108. s://doi.org/10.1007/s11302-023-09963-w

Müller C E, Namasivayam V (2021) Recommended tool compounds and drugs for blocking P2X and P2Y receptors. Purinergic Signal 17(4): 633–648. s://doi.org/10.1007/s11302-021-09813-7

Li B, Han S, Wang M, Yu Y, Ma L, Chu X, Tan Q, Zhao Q, Wu B (2023) Structural insights into signal transduction of the purinergic receptors P2Y1R and P2Y12R. Protein Cell 14(5): 382–386. s://doi.org/10.1093/procel/pwac025

Lalo U, Pankratov Y (2023) ATP-mediated signalling in the central synapses. Neuropharmacology 229: 109477. s://doi.org/10.1016/j.neuropharm.2023.109477

Shigetomi E, Sakai K, Koizumi S (2024) Extracellular ATP/adenosine dynamics in the brain and its role in health and disease. Front Cell Dev Biol 11: 1343653. s://doi.org/10.3389/fcell.2023.1343653

Menéndez Méndez A, Smith J, Engel T (2020) Neonatal seizures and purinergic signalling. Int J Mol Sci 21(21): 7832. s://doi.org/10.3390/ijms21217832

Goenaga J, Araque A, Kofuji P, Herrera Moro Chao D (2023) Calcium signaling in astrocytes and gliotransmitter release. Front Synaptic Neurosci 15: 1138577. https://doi.org/10.3389/fnsyn.2023.1138577

Lovatt D, Xu Q, Liu W, Takano T, Smith N A, Schnermann J, Tieu K, Nedergaard M (2012) Neuronal adenosine release, and not astrocytic ATP release, mediates feedback inhibition of excitatory activity. Proc Natl Acad Sci U S A 109(16): 6265–6270. s://doi.org/10.1073/pnas.1120997109

Rimbert S, Moreira J B, Xapelli S, Lévi S (2023) Role of purines in brain development, from neuronal proliferation to synaptic refinement. Neuropharmacology 237: 109640. https://doi.org/10.1016/j.neuropharm.2023.109640

Hatashita Y, Wu Z, Fujita H, Kumamoto T, Livet J, Li Y, Tanifuji M, Inoue T (2023) Spontaneous and multifaceted ATP release from astrocytes at the scale of hundreds of synapses. Glia 71(9): 2250–2265. s://doi.org/10.1002/glia.24392

Manca P, Mameli O, Caria MA, Torrejón-Escribano B, Blasi J (2014) Distribution of SNAP25, VAMP1 and VAMP2 in mature and developing deep cerebellar nuclei after estrogen administration. Neuroscience 266: 102–115. s://doi.org/10.1016/j.neuroscience.2014.02.008

Nabel A L, Teich L, Wohlfrom H, Alexandrova O, Heß M, Pecka M, Grothe B (2024) Development of myelination and axon diameter for fast and precise action potential conductance. Glia 72(4): 794–808. s://doi.org/10.1002/glia.24504

Menéndez-Méndez A, Díaz-Hernández J I, Ortega F, Gualix J, Gómez-Villafuertes R, Miras-Portugal M T (2017) Specific temporal distribution and subcellular localization of a functional vesicular nucleotide transporter (VNUT) in cerebellar granule neurons. Front Pharmacol 8: 951. s://doi.org/10.3389/fphar.2017.00951

Juvenal G, Higa G S V, Bonfim Marques L, Tessari Zampieri T, Costa Viana F J, Britto L R, Tang Y, Illes P, Di Virgilio F, Ulrich H, De Pasquale R (2024) Regulation of GABAergic neurotransmission by purinergic receptors in brain physiology and disease. Purinergic Signal 21: 149–177. s://doi.org/10.1007/s11302-024-10034-x

Zimmermann H (2021) Ectonucleoside triphosphate diphosphohydrolases and ecto-5'-nucleotidase in purinergic signaling: how the field developed and where we are now. Purinergic Signal 17(1): 117–125. s://doi.org/10.1007/s11302-020-09755-6

Todorov LD, Mihaylova-Todorova S, Westfall TD, Sneddon P, Kennedy C, Bjur RA, Westfall DP (1997) Neuronal release of soluble nucleotidases and their role in neurotransmitter inactivation. Nature 387(6628): 76–79. s://doi.org/10.1038/387076a0

Grković I, Drakulić D, Martinović J, Mitrović N (2019) Role of ectonucleotidases in synapse formation during brain development: physiological and pathological implications. Curr Neuropharmacol 17(1): 84–98. s://doi.org/10.2174/1570159X15666170518151541

Gomez-Castro F, Zappettini S, Pressey JC, Silva CG, Russeau M, Gervasi N, Figueiredo M, Montmasson C, Renner M, Canas PM, Gonçalves FQ, Alçada-Morais S, Szabó E, Rodrigues RJ, Agostinho P, Tomé AR, Caillol G, Thoumine O, Nicol X, Leterrier C, Lujan R, Tyagarajan SK, Cunha RA, Esclapez M, Bernard C, Lévi S (2021) Convergence of adenosine and GABA signaling for synapse stabilization during development. Science 374(6568): eabk2055. s://doi.org/10.1126/science.abk2055

Safiulina VF, Kasyanov AM, Sokolova E, Cherubini E, Giniatullin R (2005) ATP contributes to the generation of network-driven giant depolarizing potentials in the neonatal rat hippocampus. J Physiol 565(Pt 3): 981–992. https://doi.org/10.1113/jphysiol.2005.085621

Vassort G (2001) Adenosine 5′-triphosphate: a P2-purinergic agonist in the myocardium. Physiol Rev 81(2): 767–806. s://doi.org/10.1152/physrev.2001

Anikina TA, Sitdikov FG, Khamzina EY, Bilalova GA (2005) Role of purinoceptors in cardiac function in rats during ontogeny. Bull Exp Biol Med 140(5): 483–485. s://doi.org/10.1007/s10517-006-0002-x

Pustovit KB, Potekhina VM, Ivanova AD, Petrov AM, Abramochkin DV, Kuzmin VS (2019) Extracellular ATP and β-NAD alter electrical properties and cholinergic effects in the rat heart in age-specific manner. Purinergic Signal 15(1): 107–117. s://doi.org/10.1007/s11302-019-09645-6

Safiulina VF, Kasyanov AM, Giniatullin R, Cherubini E (2005) Adenosine down-regulates giant depolarizing potentials in the developing rat hippocampus by exerting a negative control on glutamatergic inputs. J Neurophysiol 94(4): 2797–2804. s://doi.org/10.1152/jn.00445.2005

Krnjević K (2022) Membrane current activation and inactivation during hypoxia in hippocampal neurons. In: Surviving Hypoxia, CRC Press, pp. 365–387.

Stone TW (2024) Adenosine as a neuroactive compound in the central nervous system. In: Adenosine and adenine nucleotides as regulators of cellular function, CRC Press, pp. 329–338.

Andrade-Talavera Y, Pérez-Rodríguez M, Prius-Mengual J, Rodríguez-Moreno A (2023) Neuronal and astrocyte determinants of critical periods of plasticity. Trends Neurosci 46(7):566–580. s://doi.org/10.1016/j.tins.2023.04.005

Rimbert S, Moreira JB, Xapelli S, Lévi S (2023) Role of purines in brain development, from neuronal proliferation to synaptic refinement. Neuropharmacology 237:109640. https://doi.org/10.1016/j.neuropharm.2023.109640

Cherchi F, Pugliese AM, Coppi E (2021) Oligodendrocyte precursor cell maturation: role of adenosine receptors. Neural Regen Res 16(9):1686–1692. s://doi.org/10.4103/1673-5374.306058

Ribeiro FF, Ferreira F, Rodrigues RS, Soares R, Pedro DM, Duarte-Samartinho M, Aroeira RI, Ferreiro E, Valero J, Solá S, Mira H, Sebastião AM, Xapelli S (2021) Regulation of hippocampal postnatal and adult neurogenesis by adenosine A2A receptor: Interaction with brain-derived neurotrophic factor. Stem Cells 39(10):1362–1381. s://doi.org/10.1002/stem.3421

Rodriguez-Alvarez N, Jimenez-Mateos EM, Engel T, Quinlan S, Reschke CR, Conroy RM, Bhattacharya A, Boylan GB, Henshall DC (2017) Effects of P2X7 receptor antagonists on hypoxia-induced neonatal seizures in mice. Neuropharmacology 116:351–363. s://doi.org/10.1016/j.neuropharm.2017.01.005

Rubio ME, Soto F (2001) Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21(2):641–653. s://doi.org/10.1523/JNEUROSCI.21-02-00641.2001

Henshall DC, Engel T (2015) P2X purinoceptors as a link between hyperexcitability and neuroinflammation in status epilepticus. Epilepsy Behav 49:8–12. s://doi.org/10.1016/j.yebeh.2015.02.031

Schwindt TT, Trujillo CA, Negraes PD, Lameu C, Ulrich H (2011) Directed differentiation of neural progenitors into neurons is accompanied by altered expression of P2X purinergic receptors. J Mol Neurosci 44(3):141–146. s://doi.org/10.1007/s12031-010-9417-y

Ross FM, Brodie MJ, Stone TW (1998) Modulation by adenine nucleotides of epileptiform activity in the CA3 region of rat hippocampal slices. Br J Pharmacol 123(1):71–80. s://doi.org/10.1038/sj.bjp.0701586

Pankratov YV, Lalo UV, Krishtal OA (2002) Role for P2X receptors in long-term potentiation. J Neurosci 22(19):8363–8369. s://doi.org/10.1523/JNEUROSCI.22-19-08363.2002

Smith J, Lopez-Avila BG, Engel T, Mateos EMJ, Alves M (2024) Differential expression of the metabotropic P2Y receptor family after hypoxia-induced seizures in neonates and seizure suppression via P2Y1 receptor agonism. Purinergic Signal 20(2):157–162. s://doi.org/10.1007/s11302-023-09923-4

Zhu Y, Kimelberg HK (2001) Developmental expression of metabotropic P2Y(1) and P2Y(2) receptors in freshly isolated astrocytes from rat hippocampus. J Neurochem 77(2):530–541. s://doi.org/10.1046/j.1471-4159.2001.00241.x

Rodrigues RJ, Figueira AS, Marques JM (2022) P2Y1 Receptor as a Catalyst of Brain Neurodegeneration. NeuroSci 3(4):604–615. s://doi.org/10.3390/neurosci3040043

Zhang W, Bonadiman A, Ciorraga M, Benitez MJ, Garrido JJ (2019) P2Y1 Purinergic Receptor Modulates Axon Initial Segment Initial Development. Front Cell Neurosci 13:152. s://doi.org/10.3389/fncel.2019.00152

Barańska J, Czajkowski R, Pomorski P (2017) P2Y1 Receptors – Properties and Functional Activities. Adv Exp Med Biol 1051:71–89. s://doi.org/10.1007/5584_2017_57

Felix L, Stephan J, Rose CR (2021) Astrocytes of the early postnatal brain. Eur J Neurosci 54(5):5649–5672. s://doi.org/10.1111/ejn.14780

Kukley M, Kiladze M, Tognatta R, Hans M, Swandulla D, Schramm J, Dietrich D (2008) Glial cells are born with synapses. FASEB J 22(8):2957–2969. s://doi.org/10.1096/fj.07-090985

Wang Y, Fu AKY, Ip NY (2022) Instructive roles of astrocytes in hippocampal synaptic plasticity: neuronal activity-dependent regulatory mechanisms. FEBS J 289(8):2202–2218. s://doi.org/10.1111/febs.15878

Cserép C, Pósfai B, Dénes Á (2021) Shaping Neuronal Fate: Functional Heterogeneity of Direct Microglia-Neuron Interactions. Neuron 109(2):222–240. s://doi.org/10.1016/j.neuron.2020.11.007

Cserép C, Schwarcz AD, Pósfai B, László ZI, Kellermayer A, Környei Z, Kisfali M, Nyerges M, Lele Z, Katona I, Ádám Dénes (2022) Microglial control of neuronal development via somatic purinergic junctions. Cell Rep 40(12):111369. s://doi.org/10.1016/j.celrep.2022.111369

Du Y, Brennan FH, Popovich PG, Zhou M (2022) Microglia maintain the normal structure and function of the hippocampal astrocyte network. Glia 70(7):1359–1379. s://doi.org/10.1002/glia.24179

Deivasigamani S, Miteva MT, Natale S, Gutierrez-Barragan D, Basilico B, Di Angelantonio S, Weinhard L, Molotkov D, Deb S, Pape C, Bolasco G, Galbusera A, Asari H, Gozzi A, Ragozzino D, Gross CT (2023) Microglia complement signaling promotes neuronal elimination and normal brain functional connectivity. Cereb Cortex 33(21):10750–10760. s://doi.org/10.1093/cercor/bhad313

Ferrucci L, Cantando I, Cordella F, Di Angelantonio S, Ragozzino D, Bezzi P (2023) Microglia at the Tripartite Synapse during Postnatal Development: Implications for Autism Spectrum Disorders and Schizophrenia. Cells 12(24):2827. s://doi.org/10.3390/cells12242827

Cohen JE, Fields RD (2008) Activity-dependent neuron-glial signaling by ATP and leukemia-inhibitory factor promotes hippocampal glial cell development. Neuron Glia Biol 4(1):43–55. s://doi.org/10.1017/S1740925X09000076

Lezmy J, Arancibia-Cárcamo IL, Quintela-López T, Sherman DL, Brophy PJ, Attwell D (2021) Astrocyte Ca2+-evoked ATP release regulates myelinated axon excitability and conduction speed. Science 374(6565):eabh2858. s://doi.org/10.1126/science.abh2858

Lezmy J (2023) How astrocytic ATP shapes neuronal activity and brain circuits. Curr Opin Neurobiol 79:102685. s://doi.org/10.1016/j.conb.2023.102685

Safiulina VF, Afzalov R, Khiroug L, Cherubini E, Giniatullin R (2006) Reactive oxygen species mediate the potentiating effects of ATP on GABAergic synaptic transmission in the immature hippocampus. J Biol Chem 281(33):23464–23470. s://doi.org/10.1074/jbc.M601627200

Rahman MM, Islam MR, Yamin M, Islam MM, Sarker MT, Meem AFK, Akter A, Emran TB, Cavalu S, Sharma R (2022) Emerging Role of Neuron-Glia in Neurological Disorders: At a Glance. Oxid Med Cell Longev 2022:3201644. s://doi.org/10.1155/2022/3201644

Vargas E, Petrou S, Reid CA (2013) Genetic and pharmacological modulation of giant depolarizing potentials in the neonatal hippocampus associates with increased seizure susceptibility. J Physiol 591(1):57–65. s://doi.org/10.1113/jphysiol.2012.234674

Beamer E, Kuchukulla M, Boison D, Engel T (2021) ATP and adenosine – Two players in the control of seizures and epilepsy development. Prog Neurobiol 204:102105. s://doi.org/10.1016/j.pneurobio.2021.102105

Rodriguez-Alvarez N, Jimenez-Mateos EM, Engel T, Quinlan S, Reschke CR, Conroy RM, Bhattacharya A, Boylan GB, Henshall DC (2017) Effects of P2X7 receptor antagonists on hypoxia-induced neonatal seizures in mice. Neuropharmacology 116:351–363. s://doi.org/10.1016/j.neuropharm.2017.01.005

Engel T (2023) The P2X7 Receptor as a Mechanistic Biomarker for Epilepsy. Int J Mol Sci 24(6):5410. s://doi.org/10.3390/ijms24065410

Del Puerto A, Wandosell F, Garrido JJ (2013) Neuronal and glial purinergic receptors functions in neuron development and brain disease. Front Cell Neurosci 7:197. s://doi.org/10.3389/fncel.2013.00197