Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Astrocytes and Memory: Implications for the Treatment of Memory-related Disorders

Author(s): Juan Wang, Ping Cheng, Yan Qu and Guoqi Zhu*

Volume 22, Issue 13, 2024

Published on: 29 January, 2024

Page: [2217 - 2239] Pages: 23

DOI: 10.2174/1570159X22666240128102039

Price: $65

Abstract

Memory refers to the imprint accumulated in the brain by life experiences and represents the basis for humans to engage in advanced psychological activities such as thinking and imagination. Previously, research activities focused on memory have always targeted neurons. However, in addition to neurons, astrocytes are also involved in the encoding, consolidation, and extinction of memory. In particular, astrocytes are known to affect the recruitment and function of neurons at the level of local synapses and brain networks. Moreover, the involvement of astrocytes in memory and memory-related disorders, especially in Alzheimer’s disease (AD) and post-traumatic stress disorder (PTSD), has been investigated extensively. In this review, we describe the unique contributions of astrocytes to synaptic plasticity and neuronal networks and discuss the role of astrocytes in different types of memory processing. In addition, we also explore the roles of astrocytes in the pathogenesis of memory-related disorders, such as AD, brain aging, PTSD and addiction, thus suggesting that targeting astrocytes may represent a potential strategy to treat memory-related neurological diseases. In conclusion, this review emphasizes that thinking from the perspective of astrocytes will provide new ideas for the diagnosis and therapy of memory-related neurological disorders.

« Previous Next »
Graphical Abstract

[1]
Haim, L.B.; Rowitch, D.H. Functional diversity of astrocytes in neural circuit regulation. Nat. Rev. Neurosci., 2017, 18(1), 31-41.
[http://dx.doi.org/10.1038/nrn.2016.159] [PMID: 27904142]
[2]
Chung, W.S.; Allen, N.J.; Eroglu, C. Astrocytes control synapse formation, function, and elimination. Cold Spring Harb. Perspect. Biol., 2015, 7(9), a020370.
[http://dx.doi.org/10.1101/cshperspect.a020370] [PMID: 25663667]
[3]
Araque, A.; Parpura, V.; Sanzgiri, R.P.; Haydon, P.G. Tripartite synapses: Glia, the unacknowledged partner. Trends Neurosci., 1999, 22(5), 208-215.
[http://dx.doi.org/10.1016/S0166-2236(98)01349-6] [PMID: 10322493]
[4]
Khakh, B.S.; Deneen, B. The emerging nature of astrocyte diversity. Annu. Rev. Neurosci., 2019, 42(1), 187-207.
[http://dx.doi.org/10.1146/annurev-neuro-070918-050443] [PMID: 31283899]
[5]
Verkhratsky, A.; Nedergaard, M. Physiology of astroglia. Physiol. Rev., 2018, 98(1), 239-389.
[http://dx.doi.org/10.1152/physrev.00042.2016] [PMID: 29351512]
[6]
Akther, S.; Hirase, H. Assessment of astrocytes as a mediator of memory and learning in rodents. Glia, 2022, 70(8), 1484-1505.
[http://dx.doi.org/10.1002/glia.24099] [PMID: 34582594]
[7]
Khaspekov, L.G.; Frumkina, L.E. Molecular mechanisms of astrocyte involvement in synaptogenesis and brain synaptic plasticity. Biochemistry, 2023, 88(4), 502-514.
[http://dx.doi.org/10.1134/S0006297923040065] [PMID: 37080936]
[8]
Dienel, G.A.; Schousboe, A.; McKenna, M.C.; Rothman, D.L. A tribute to Leif Hertz: The historical context of his pioneering studies of the roles of astrocytes in brain energy metabolism, neurotransmission, cognitive functions, and pharmacology identifies important, unresolved topics for future studies. J. Neurochem., 2023, 15812.
[http://dx.doi.org/10.1111/jnc.15812] [PMID: 36928655]
[9]
Chen, Y.H.; Jin, S.Y.; Yang, J.M.; Gao, T.M. The memory orchestra: Contribution of astrocytes. Neurosci. Bull., 2023, 39(3), 409-424.
[http://dx.doi.org/10.1007/s12264-023-01024-x] [PMID: 36738435]
[10]
Endo, F.; Kasai, A.; Soto, J.S.; Yu, X.; Qu, Z.; Hashimoto, H.; Gradinaru, V.; Kawaguchi, R.; Khakh, B.S. Molecular basis of astrocyte diversity and morphology across the CNS in health and disease. Science, 2022, 378(6619), eadc9020.
[http://dx.doi.org/10.1126/science.adc9020] [PMID: 36378959]
[11]
Arranz, A.M.; De Strooper, B. The role of astroglia in Alzheimer’s disease: Pathophysiology and clinical implications. Lancet Neurol., 2019, 18(4), 406-414.
[http://dx.doi.org/10.1016/S1474-4422(18)30490-3] [PMID: 30795987]
[12]
Jones, M.E.; Lebonville, C.L.; Paniccia, J.E.; Balentine, M.E.; Reissner, K.J.; Lysle, D.T. Hippocampal interleukin-1 mediates stress-enhanced fear learning: A potential role for astrocyte-derived interleukin-1β. Brain Behav. Immun., 2018, 67, 355-363.
[http://dx.doi.org/10.1016/j.bbi.2017.09.016] [PMID: 28963000]
[13]
Yang, J.; Chen, J.; Liu, Y.; Chen, K.H.; Baraban, J.M.; Qiu, Z. Ventral tegmental area astrocytes modulate cocaine reward by tonically releasing GABA. Neuron, 2023, 111(7), 1104-1117.e6.
[http://dx.doi.org/10.1016/j.neuron.2022.12.033] [PMID: 36681074]
[14]
Lee, S.H.; Mak, A.; Verheijen, M.H.G. Comparative assessment of the effects of DREADDs and endogenously expressed GPCRs in hippocampal astrocytes on synaptic activity and memory. Front. Cell. Neurosci., 2023, 17, 1159756.
[http://dx.doi.org/10.3389/fncel.2023.1159756] [PMID: 37051110]
[15]
Goshen, I. The optogenetic revolution in memory research. Trends Neurosci., 2014, 37(9), 511-522.
[http://dx.doi.org/10.1016/j.tins.2014.06.002] [PMID: 25022518]
[16]
Yu, X.; Nagai, J.; Khakh, B.S. Improved tools to study astrocytes. Nat. Rev. Neurosci., 2020, 21(3), 121-138.
[http://dx.doi.org/10.1038/s41583-020-0264-8] [PMID: 32042146]
[17]
Savtchenko, L.P.; Bard, L.; Jensen, T.P.; Reynolds, J.P.; Kraev, I.; Medvedev, N.; Stewart, M.G.; Henneberger, C.; Rusakov, D.A. Disentangling astroglial physiology with a realistic cell model in silico. Nat. Commun., 2018, 9(1), 3554.
[http://dx.doi.org/10.1038/s41467-018-05896-w] [PMID: 30177844]
[18]
Verkhratsky, A.; Reyes, R.C.; Parpura, V. TRP channels coordinate ion signalling in astroglia. Rev. Physiol. Biochem. Pharmacol., 2014, 166, 1-22.
[PMID: 23784619]
[19]
Semyanov, A.; Henneberger, C.; Agarwal, A. Making sense of astrocytic calcium signals - from acquisition to interpretation. Nat. Rev. Neurosci., 2020, 21(10), 551-564.
[http://dx.doi.org/10.1038/s41583-020-0361-8] [PMID: 32873937]
[20]
Agarwal, A.; Wu, P.H.; Hughes, E.G.; Fukaya, M.; Tischfield, M.A.; Langseth, A.J.; Wirtz, D.; Bergles, D.E. Transient opening of the mitochondrial permeability transition pore induces microdomain calcium transients in astrocyte processes. Neuron, 2017, 93(3), 587-605.e7.
[http://dx.doi.org/10.1016/j.neuron.2016.12.034] [PMID: 28132831]
[21]
Bojarskaite, L.; Bjørnstad, D.M.; Pettersen, K.H.; Cunen, C.; Hermansen, G.H.; Åbjørsbråten, K.S.; Chambers, A.R.; Sprengel, R.; Vervaeke, K.; Tang, W.; Enger, R.; Nagelhus, E.A. Astrocytic Ca2+ signaling is reduced during sleep and is involved in the regulation of slow wave sleep. Nat. Commun., 2020, 11(1), 3240.
[http://dx.doi.org/10.1038/s41467-020-17062-2] [PMID: 32632168]
[22]
Wu, Y.W.; Gordleeva, S.; Tang, X.; Shih, P.Y.; Dembitskaya, Y.; Semyanov, A. Morphological profile determines the frequency of spontaneous calcium events in astrocytic processes. Glia, 2019, 67(2), 246-262.
[http://dx.doi.org/10.1002/glia.23537] [PMID: 30565755]
[23]
Denizot, A.; Arizono, M.; Nägerl, U.V.; Soula, H.; Berry, H. Simulation of calcium signaling in fine astrocytic processes: Effect of spatial properties on spontaneous activity. PLOS Comput. Biol., 2019, 15(8), e1006795.
[http://dx.doi.org/10.1371/journal.pcbi.1006795] [PMID: 31425510]
[24]
Lines, J.; Martin, E.D.; Kofuji, P.; Aguilar, J.; Araque, A. Astrocytes modulate sensory-evoked neuronal network activity. Nat. Commun., 2020, 11(1), 3689.
[http://dx.doi.org/10.1038/s41467-020-17536-3] [PMID: 32704144]
[25]
Boddum, K.; Jensen, T.P.; Magloire, V.; Kristiansen, U.; Rusakov, D.A.; Pavlov, I.; Walker, M.C. Astrocytic GABA transporter activity modulates excitatory neurotransmission. Nat. Commun., 2016, 7(1), 13572.
[http://dx.doi.org/10.1038/ncomms13572] [PMID: 27886179]
[26]
Kofuji, P.; Araque, A. G-protein-coupled receptors in astrocyte-neuron communication. Neuroscience, 2021, 456, 71-84.
[http://dx.doi.org/10.1016/j.neuroscience.2020.03.025] [PMID: 32224231]
[27]
Bazargani, N.; Attwell, D. Astrocyte calcium signaling: The third wave. Nat. Neurosci., 2016, 19(2), 182-189.
[http://dx.doi.org/10.1038/nn.4201] [PMID: 26814587]
[28]
Volterra, A.; Liaudet, N.; Savtchouk, I. Astrocyte Ca2+ signalling: An unexpected complexity. Nat. Rev. Neurosci., 2014, 15(5), 327-335.
[http://dx.doi.org/10.1038/nrn3725] [PMID: 24739787]
[29]
Srinivasan, R.; Huang, B.S.; Venugopal, S.; Johnston, A.D.; Chai, H.; Zeng, H.; Golshani, P.; Khakh, B.S. Ca2+ signaling in astrocytes from Ip3r2−/− mice in brain slices and during startle responses in vivo. Nat. Neurosci., 2015, 18(5), 708-717.
[http://dx.doi.org/10.1038/nn.4001] [PMID: 25894291]
[30]
Semyanov, A. Spatiotemporal pattern of calcium activity in astrocytic network. Cell Calcium, 2019, 78, 15-25.
[http://dx.doi.org/10.1016/j.ceca.2018.12.007] [PMID: 30579813]
[31]
Arizono, M.; Inavalli, V.V.G.K.; Panatier, A.; Pfeiffer, T.; Angibaud, J.; Levet, F.; Ter Veer, M.J.T.; Stobart, J.; Bellocchio, L.; Mikoshiba, K.; Marsicano, G.; Weber, B.; Oliet, S.H.R.; Nägerl, U.V. Structural basis of astrocytic Ca2+ signals at tripartite synapses. Nat. Commun., 2020, 11(1), 1906.
[http://dx.doi.org/10.1038/s41467-020-15648-4] [PMID: 32312988]
[32]
Georgiou, L.; Echeverría, A.; Georgiou, A.; Kuhn, B. Ca 2+ activity maps of astrocytes tagged by axoastrocytic AAV transfer. Sci. Adv., 2022, 8(6), eabe5371.
[http://dx.doi.org/10.1126/sciadv.abe5371] [PMID: 35138891]
[33]
Stobart, J.L.; Ferrari, K.D.; Barrett, M.J.P.; Glück, C.; Stobart, M.J.; Zuend, M.; Weber, B. Cortical circuit activity evokes rapid astrocyte calcium signals on a similar timescale to neurons. Neuron, 2018, 98(4), 726-735.e4.
[http://dx.doi.org/10.1016/j.neuron.2018.03.050] [PMID: 29706581]
[34]
Wang, Y.; DelRosso, N.V.; Vaidyanathan, T.V.; Cahill, M.K.; Reitman, M.E.; Pittolo, S.; Mi, X.; Yu, G.; Poskanzer, K.E. Accurate quantification of astrocyte and neurotransmitter fluorescence dynamics for single-cell and population-level physiology. Nat. Neurosci., 2019, 22(11), 1936-1944.
[http://dx.doi.org/10.1038/s41593-019-0492-2] [PMID: 31570865]
[35]
Zhu, G.; Liu, Y.; Wang, Y.; Bi, X.; Baudry, M. Different patterns of electrical activity lead to long-term potentiation by activating different intracellular pathways. J. Neurosci., 2015, 35(2), 621-633.
[http://dx.doi.org/10.1523/JNEUROSCI.2193-14.2015] [PMID: 25589756]
[36]
Zhu, G.; Briz, V.; Seinfeld, J.; Liu, Y.; Bi, X.; Baudry, M. Calpain-1 deletion impairs mGluR-dependent LTD and fear memory extinction. Sci. Rep., 2017, 7(1), 42788.
[http://dx.doi.org/10.1038/srep42788] [PMID: 28202907]
[37]
Frankland, P.W.; Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci., 2005, 6(2), 119-130.
[http://dx.doi.org/10.1038/nrn1607] [PMID: 15685217]
[38]
Magee, J.C.; Grienberger, C. Synaptic plasticity forms and functions. Annu. Rev. Neurosci., 2020, 43(1), 95-117.
[http://dx.doi.org/10.1146/annurev-neuro-090919-022842] [PMID: 32075520]
[39]
Allen, N.J.; Lyons, D.A. Glia as architects of central nervous system formation and function. Science, 2018, 362(6411), 181-185.
[http://dx.doi.org/10.1126/science.aat0473] [PMID: 30309945]
[40]
Bliss, T.V.P.; Lømo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol., 1973, 232(2), 331-356.
[http://dx.doi.org/10.1113/jphysiol.1973.sp010273] [PMID: 4727084]
[41]
Malenka, R.C.; Bear, M.F. LTP and LTD: An embarrassment of riches. Neuron, 2004, 44(1), 5-21.
[http://dx.doi.org/10.1016/j.neuron.2004.09.012] [PMID: 15450156]
[42]
Nguyen, P.V.; Abel, T.; Kandel, E.R. Requirement of a critical period of transcription for induction of a late phase of LTP. Science, 1994, 265(5175), 1104-1107.
[http://dx.doi.org/10.1126/science.8066450] [PMID: 8066450]
[43]
Sherwood, M.W.; Arizono, M.; Hisatsune, C.; Bannai, H.; Ebisui, E.; Sherwood, J.L.; Panatier, A.; Oliet, S.H.R.; Mikoshiba, K. Astrocytic IP3Rs: Contribution to Ca2+ signalling and hippocampal LTP. Glia, 2017, 65(3), 502-513.
[http://dx.doi.org/10.1002/glia.23107] [PMID: 28063222]
[44]
Navarrete, M.; Perea, G.; de Sevilla, D.F.; Gómez-Gonzalo, M.; Núñez, A.; Martín, E.D.; Araque, A. Astrocytes mediate in vivo cholinergic-induced synaptic plasticity. PLoS Biol., 2012, 10(2), e1001259.
[http://dx.doi.org/10.1371/journal.pbio.1001259] [PMID: 22347811]
[45]
Liu, J.H.; Zhang, M.; Wang, Q.; Wu, D.Y.; Jie, W.; Hu, N.Y.; Lan, J.Z.; Zeng, K.; Li, S.J.; Li, X.W.; Yang, J.M.; Gao, T.M. Distinct roles of astroglia and neurons in synaptic plasticity and memory. Mol. Psychiatry, 2022, 27(2), 873-885.
[http://dx.doi.org/10.1038/s41380-021-01332-6] [PMID: 34642458]
[46]
Requie, L.M.; Gómez-Gonzalo, M.; Speggiorin, M.; Managò, F.; Melone, M.; Congiu, M.; Chiavegato, A.; Lia, A.; Zonta, M.; Losi, G.; Henriques, V.J.; Pugliese, A.; Pacinelli, G.; Marsicano, G.; Papaleo, F.; Muntoni, A.L.; Conti, F.; Carmignoto, G. Astrocytes mediate long-lasting synaptic regulation of ventral tegmental area dopamine neurons. Nat. Neurosci., 2022, 25(12), 1639-1650.
[http://dx.doi.org/10.1038/s41593-022-01193-4] [PMID: 36396976]
[47]
Henneberger, C.; Papouin, T.; Oliet, S.H.R.; Rusakov, D.A. Long-term potentiation depends on release of d-serine from astrocytes. Nature, 2010, 463(7278), 232-236.
[http://dx.doi.org/10.1038/nature08673] [PMID: 20075918]
[48]
Mothet, J.P.; Parent, A.T.; Wolosker, H.; Brady, R.O., Jr; Linden, D.J.; Ferris, C.D.; Rogawski, M.A.; Snyder, S.H. D -Serine is an endogenous ligand for the glycine site of the N -methyl- D -aspartate receptor. Proc. Natl. Acad. Sci., 2000, 97(9), 4926-4931.
[http://dx.doi.org/10.1073/pnas.97.9.4926] [PMID: 10781100]
[49]
Coyle, J.T.; Balu, D.; Wolosker, H. d-serine, the shape-shifting NMDA receptor co-agonist. Neurochem. Res., 2020, 45(6), 1344-1353.
[http://dx.doi.org/10.1007/s11064-020-03014-1] [PMID: 32189130]
[50]
Wolosker, H.; Balu, D.T.; Coyle, J.T. The rise and fall of the d -serine-mediated gliotransmission hypothesis. Trends Neurosci., 2016, 39(11), 712-721.
[http://dx.doi.org/10.1016/j.tins.2016.09.007] [PMID: 27742076]
[51]
Papouin, T.; Dunphy, J.M.; Tolman, M.; Dineley, K.T.; Haydon, P.G. Septal cholinergic neuromodulation tunes the astrocyte-dependent gating of hippocampal NMDA receptors to wakefulness. Neuron, 2017, 94(4), 840-854.e7.
[http://dx.doi.org/10.1016/j.neuron.2017.04.021] [PMID: 28479102]
[52]
Koh, W.; Park, M.; Chun, Y.E.; Lee, J.; Shim, H.S.; Park, M.G.; Kim, S.; Sa, M.; Joo, J.; Kang, H.; Oh, S.J.; Woo, J.; Chun, H.; Lee, S.E.; Hong, J.; Feng, J.; Li, Y.; Ryu, H.; Cho, J.; Lee, C.J. Astrocytes render memory flexible by releasing D-serine and regulating NMDA receptor tone in the hippocampus. Biol. Psychiatry, 2022, 91(8), 740-752.
[http://dx.doi.org/10.1016/j.biopsych.2021.10.012] [PMID: 34952697]
[53]
Huang, A.Y.S.; Woo, J.; Sardar, D.; Lozzi, B.; Bosquez Huerta, N.A.; Lin, C.C.J.; Felice, D.; Jain, A.; Paulucci-Holthauzen, A.; Deneen, B. Region-specific transcriptional control of astrocyte function oversees local circuit activities. Neuron, 2020, 106(6), 992-1008.e9.
[http://dx.doi.org/10.1016/j.neuron.2020.03.025] [PMID: 32320644]
[54]
Suzuki, A.; Stern, S.A.; Bozdagi, O.; Huntley, G.W.; Walker, R.H.; Magistretti, P.J.; Alberini, C.M. Astrocyte-neuron lactate transport is required for long-term memory formation. Cell, 2011, 144(5), 810-823.
[http://dx.doi.org/10.1016/j.cell.2011.02.018] [PMID: 21376239]
[55]
González-Gutiérrez, A.; Ibacache, A.; Esparza, A.; Barros, L.F.; Sierralta, J. Neuronal lactate levels depend on glia‐derived lactate during high brain activity in Drosophila. Glia, 2020, 68(6), 1213-1227.
[http://dx.doi.org/10.1002/glia.23772] [PMID: 31876077]
[56]
Vezzoli, E.; Calì, C.; De Roo, M.; Ponzoni, L.; Sogne, E.; Gagnon, N.; Francolini, M.; Braida, D.; Sala, M.; Muller, D.; Falqui, A.; Magistretti, P.J. Ultrastructural evidence for a role of astrocytes and glycogen-derived lactate in learning-dependent synaptic stabilization. Cereb. Cortex, 2020, 30(4), 2114-2127.
[http://dx.doi.org/10.1093/cercor/bhz226] [PMID: 31807747]
[57]
Descalzi, G.; Gao, V.; Steinman, M.Q.; Suzuki, A.; Alberini, C.M. Lactate from astrocytes fuels learning-induced mRNA translation in excitatory and inhibitory neurons. Commun. Biol., 2019, 2(1), 247.
[http://dx.doi.org/10.1038/s42003-019-0495-2] [PMID: 31286064]
[58]
Herkenham, M.; Lynn, A.B.; Little, M.D.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci., 1990, 87(5), 1932-1936.
[http://dx.doi.org/10.1073/pnas.87.5.1932] [PMID: 2308954]
[59]
Navarrete, M.; Araque, A. Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron, 2010, 68(1), 113-126.
[http://dx.doi.org/10.1016/j.neuron.2010.08.043] [PMID: 20920795]
[60]
Robin, L.M.; Oliveira da Cruz, J.F.; Langlais, V.C.; Martin-Fernandez, M.; Metna-Laurent, M.; Busquets-Garcia, A.; Bellocchio, L.; Soria-Gomez, E.; Papouin, T.; Varilh, M.; Sherwood, M.W.; Belluomo, I.; Balcells, G.; Matias, I.; Bosier, B.; Drago, F.; Van Eeckhaut, A.; Smolders, I.; Georges, F.; Araque, A.; Panatier, A.; Oliet, S.H.R.; Marsicano, G. Astroglial CB1 receptors determine synaptic d-serine availability to enable recognition memory. Neuron, 2018, 98(5), 935-944.e5.
[http://dx.doi.org/10.1016/j.neuron.2018.04.034] [PMID: 29779943]
[61]
Zhou, Z.; Okamoto, K.; Onodera, J.; Hiragi, T.; Andoh, M.; Ikawa, M.; Tanaka, K.F.; Ikegaya, Y.; Koyama, R. Astrocytic cAMP modulates memory via synaptic plasticity. Proc. Natl. Acad. Sci., 2021, 118(3), e2016584118.
[http://dx.doi.org/10.1073/pnas.2016584118] [PMID: 33452135]
[62]
Chi, S.; Cui, Y.; Wang, H.; Jiang, J.; Zhang, T.; Sun, S.; Zhou, Z.; Zhong, Y.; Xiao, B. Astrocytic Piezo1-mediated mechanotransduction determines adult neurogenesis and cognitive functions. Neuron, 2022, 110(18), 2984-2999.e8.
[http://dx.doi.org/10.1016/j.neuron.2022.07.010] [PMID: 35963237]
[63]
Henneberger, C.; Bard, L.; Panatier, A.; Reynolds, J.P.; Kopach, O.; Medvedev, N.I.; Minge, D.; Herde, M.K.; Anders, S.; Kraev, I.; Heller, J.P.; Rama, S.; Zheng, K.; Jensen, T.P.; Sanchez-Romero, I.; Jackson, C.J.; Janovjak, H.; Ottersen, O.P.; Nagelhus, E.A.; Oliet, S.H.R.; Stewart, M.G.; Nägerl, U.V.; Rusakov, D.A. LTP induction boosts glutamate spillover by driving withdrawal of perisynaptic astroglia. Neuron, 2020, 108(5), 919-936.e11.
[http://dx.doi.org/10.1016/j.neuron.2020.08.030] [PMID: 32976770]
[64]
Vignoli, B.; Sansevero, G.; Sasi, M.; Rimondini, R.; Blum, R.; Bonaldo, V.; Biasini, E.; Santi, S.; Berardi, N.; Lu, B.; Canossa, M. Astrocytic microdomains from mouse cortex gain molecular control over long-term information storage and memory retention. Commun. Biol., 2021, 4(1), 1152.
[http://dx.doi.org/10.1038/s42003-021-02678-x] [PMID: 34611268]
[65]
Dudek, S.M.; Bear, M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci., 1992, 89(10), 4363-4367.
[http://dx.doi.org/10.1073/pnas.89.10.4363] [PMID: 1350090]
[66]
Han, J.; Kesner, P.; Metna-Laurent, M.; Duan, T.; Xu, L.; Georges, F.; Koehl, M.; Abrous, D.N.; Mendizabal-Zubiaga, J.; Grandes, P.; Liu, Q.; Bai, G.; Wang, W.; Xiong, L.; Ren, W.; Marsicano, G.; Zhang, X. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD. Cell, 2012, 148(5), 1039-1050.
[http://dx.doi.org/10.1016/j.cell.2012.01.037] [PMID: 22385967]
[67]
Navarrete, M.; Araque, A. Endocannabinoids mediate neuron-astrocyte communication. Neuron, 2008, 57(6), 883-893.
[http://dx.doi.org/10.1016/j.neuron.2008.01.029] [PMID: 18367089]
[68]
Pinto-Duarte, A.; Roberts, A.J.; Ouyang, K.; Sejnowski, T.J. Impairments in remote memory caused by the lack of Type 2 IP 3 receptors. Glia, 2019, 67(10), 1976-1989.
[http://dx.doi.org/10.1002/glia.23679] [PMID: 31348567]
[69]
Navarrete, M.; Cuartero, M.I.; Palenzuela, R.; Draffin, J.E.; Konomi, A.; Serra, I.; Colié, S.; Castaño-Castaño, S.; Hasan, M.T.; Nebreda, Á.R.; Esteban, J.A. Astrocytic p38α MAPK drives NMDA receptor-dependent long-term depression and modulates long-term memory. Nat. Commun., 2019, 10(1), 2968.
[http://dx.doi.org/10.1038/s41467-019-10830-9] [PMID: 31273206]
[70]
Soto, M.; Cai, W.; Konishi, M.; Kahn, C.R. Insulin signaling in the hippocampus and amygdala regulates metabolism and neurobehavior. Proc. Natl. Acad. Sci., 2019, 116(13), 6379-6384.
[http://dx.doi.org/10.1073/pnas.1817391116] [PMID: 30765523]
[71]
Noriega-Prieto, J.A.; Maglio, L.E.; Zegarra-Valdivia, J.A.; Pignatelli, J.; Fernandez, A.M.; Martinez-Rachadell, L.; Fernandes, J.; Núñez, Á.; Araque, A.; Torres-Alemán, I.; Fernández de Sevilla, D. Astrocytic IGF-IRs induce adenosine-mediated inhibitory downregulation and improve sensory discrimination. J. Neurosci., 2021, 41(22), 4768-4781.
[http://dx.doi.org/10.1523/JNEUROSCI.0005-21.2021] [PMID: 33911021]
[72]
Brzosko, Z.; Mierau, S.B.; Paulsen, O. Neuromodulation of spike-timing-dependent plasticity: Past, present, and future. Neuron, 2019, 103(4), 563-581.
[http://dx.doi.org/10.1016/j.neuron.2019.05.041] [PMID: 31437453]
[73]
Falcón-Moya, R.; Pérez-Rodríguez, M.; Prius-Mengual, J.; Andrade-Talavera, Y.; Arroyo-García, L.E.; Pérez-Artés, R.; Mateos-Aparicio, P.; Guerra-Gomes, S.; Oliveira, J.F.; Flores, G.; Rodríguez-Moreno, A. Astrocyte-mediated switch in spike timing-dependent plasticity during hippocampal development. Nat. Commun., 2020, 11(1), 4388.
[http://dx.doi.org/10.1038/s41467-020-18024-4] [PMID: 32873805]
[74]
Martínez-Gallego, I.; Pérez-Rodríguez, M.; Coatl-Cuaya, H.; Flores, G.; Rodríguez-Moreno, A. Adenosine and astrocytes determine the developmental dynamics of spike timing-dependent plasticity in the somatosensory cortex. J. Neurosci., 2022, 42(31), 6038-6052.
[http://dx.doi.org/10.1523/JNEUROSCI.0115-22.2022] [PMID: 35768208]
[75]
Min, R.; Nevian, T. Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat. Neurosci., 2012, 15(5), 746-753.
[http://dx.doi.org/10.1038/nn.3075] [PMID: 22446881]
[76]
Jones, E.V.; Bouvier, D.S. Astrocyte-secreted matricellular proteins in CNS remodelling during development and disease. Neural Plast., 2014, 2014, 1-12.
[http://dx.doi.org/10.1155/2014/321209] [PMID: 24551460]
[77]
Risher, W.C.; Kim, N.; Koh, S.; Choi, J.E.; Mitev, P.; Spence, E.F.; Pilaz, L.J.; Wang, D.; Feng, G.; Silver, D.L.; Soderling, S.H.; Yin, H.H.; Eroglu, C. Thrombospondin receptor α2δ-1 promotes synaptogenesis and spinogenesis via postsynaptic Rac1. J. Cell Biol., 2018, 217(10), 3747-3765.
[http://dx.doi.org/10.1083/jcb.201802057] [PMID: 30054448]
[78]
Takano, T.; Wallace, J.T.; Baldwin, K.T.; Purkey, A.M.; Uezu, A.; Courtland, J.L.; Soderblom, E.J.; Shimogori, T.; Maness, P.F.; Eroglu, C.; Soderling, S.H. Chemico-genetic discovery of astrocytic control of inhibition in vivo. Nature, 2020, 588(7837), 296-302.
[http://dx.doi.org/10.1038/s41586-020-2926-0] [PMID: 33177716]
[79]
Chung, W.S.; Clarke, L.E.; Wang, G.X.; Stafford, B.K.; Sher, A.; Chakraborty, C.; Joung, J.; Foo, L.C.; Thompson, A.; Chen, C.; Smith, S.J.; Barres, B.A. Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature, 2013, 504(7480), 394-400.
[http://dx.doi.org/10.1038/nature12776] [PMID: 24270812]
[80]
Lee, J.H.; Kim, J.; Noh, S.; Lee, H.; Lee, S.Y.; Mun, J.Y.; Park, H.; Chung, W.S. Astrocytes phagocytose adult hippocampal synapses for circuit homeostasis. Nature, 2021, 590(7847), 612-617.
[http://dx.doi.org/10.1038/s41586-020-03060-3] [PMID: 33361813]
[81]
Vainchtein, I.D.; Chin, G.; Cho, F.S.; Kelley, K.W.; Miller, J.G.; Chien, E.C.; Liddelow, S.A.; Nguyen, P.T.; Nakao-Inoue, H.; Dorman, L.C.; Akil, O.; Joshita, S.; Barres, B.A.; Paz, J.T.; Molofsky, A.B.; Molofsky, A.V. Astrocyte-derived interleukin-33 promotes microglial synapse engulfment and neural circuit development. Science, 2018, 359(6381), 1269-1273.
[http://dx.doi.org/10.1126/science.aal3589] [PMID: 29420261]
[82]
Wang, Y.; Fu, W.Y.; Cheung, K.; Hung, K.W.; Chen, C.; Geng, H.; Yung, W.H.; Qu, J.Y.; Fu, A.K.Y.; Ip, N.Y. Astrocyte-secreted IL-33 mediates homeostatic synaptic plasticity in the adult hippocampus. Proc. Natl. Acad. Sci., 2021, 118(1), e2020810118.
[http://dx.doi.org/10.1073/pnas.2020810118] [PMID: 33443211]
[83]
Koeppen, J.; Nguyen, A.Q.; Nikolakopoulou, A.M.; Garcia, M.; Hanna, S.; Woodruff, S.; Figueroa, Z.; Obenaus, A.; Ethell, I.M. Functional consequences of synapse remodeling following astrocyte-specific regulation of ephrin-B1 in the adult hippocampus. J. Neurosci., 2018, 38(25), 5710-5726.
[http://dx.doi.org/10.1523/JNEUROSCI.3618-17.2018] [PMID: 29793972]
[84]
Tan, Z.; Liu, Y.; Xi, W.; Lou, H.; Zhu, L.; Guo, Z.; Mei, L.; Duan, S. Glia-derived ATP inversely regulates excitability of pyramidal and CCK-positive neurons. Nat. Commun., 2017, 8(1), 13772.
[http://dx.doi.org/10.1038/ncomms13772] [PMID: 28128211]
[85]
Poskanzer, K.E.; Yuste, R. Astrocytes regulate cortical state switching in vivo. Proc. Natl. Acad. Sci., 2016, 113(19), E2675-E2684.
[http://dx.doi.org/10.1073/pnas.1520759113] [PMID: 27122314]
[86]
Ji, D.; Wilson, M.A. Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci., 2007, 10(1), 100-107.
[http://dx.doi.org/10.1038/nn1825] [PMID: 17173043]
[87]
Lee, H.S.; Ghetti, A.; Pinto-Duarte, A.; Wang, X.; Dziewczapolski, G.; Galimi, F.; Huitron-Resendiz, S.; Piña-Crespo, J.C.; Roberts, A.J.; Verma, I.M.; Sejnowski, T.J.; Heinemann, S.F. Astrocytes contribute to gamma oscillations and recognition memory. Proc. Natl. Acad. Sci., 2014, 111(32), E3343-E3352.
[http://dx.doi.org/10.1073/pnas.1410893111] [PMID: 25071179]
[88]
Brockett, A.T.; Kane, G.A.; Monari, P.K.; Briones, B.A.; Vigneron, P.A.; Barber, G.A.; Bermudez, A.; Dieffenbach, U.; Kloth, A.D.; Buschman, T.J.; Gould, E. Evidence supporting a role for astrocytes in the regulation of cognitive flexibility and neuronal oscillations through the Ca2+ binding protein S100β. PLoS One, 2018, 13(4), e0195726.
[http://dx.doi.org/10.1371/journal.pone.0195726] [PMID: 29664924]
[89]
Sardinha, V.M.; Guerra-Gomes, S.; Caetano, I.; Tavares, G.; Martins, M.; Reis, J.S.; Correia, J.S.; Teixeira-Castro, A.; Pinto, L.; Sousa, N.; Oliveira, J.F. Astrocytic signaling supports hippocampal–prefrontal theta synchronization and cognitive function. Glia, 2017, 65(12), 1944-1960.
[http://dx.doi.org/10.1002/glia.23205] [PMID: 28885722]
[90]
Mederos, S.; Sánchez-Puelles, C.; Esparza, J.; Valero, M.; Ponomarenko, A.; Perea, G. GABAergic signaling to astrocytes in the prefrontal cortex sustains goal-directed behaviors. Nat. Neurosci., 2021, 24(1), 82-92.
[http://dx.doi.org/10.1038/s41593-020-00752-x] [PMID: 33288910]
[91]
Luo, L. Architectures of neuronal circuits. Science, 2021, 373(6559), eabg7285.
[http://dx.doi.org/10.1126/science.abg7285] [PMID: 34516844]
[92]
Martin-Fernandez, M.; Jamison, S.; Robin, L.M.; Zhao, Z.; Martin, E.D.; Aguilar, J.; Benneyworth, M.A.; Marsicano, G.; Araque, A. Synapse-specific astrocyte gating of amygdala-related behavior. Nat. Neurosci., 2017, 20(11), 1540-1548.
[http://dx.doi.org/10.1038/nn.4649] [PMID: 28945222]
[93]
Serra, I.; Esparza, J.; Delgado, L.; Martín-Monteagudo, C.; Puigròs, M.; Podlesniy, P.; Trullás, R.; Navarrete, M. Ca2+-modulated photoactivatable imaging reveals neuron-astrocyte glutamatergic circuitries within the nucleus accumbens. Nat. Commun., 2022, 13(1), 5272.
[http://dx.doi.org/10.1038/s41467-022-33020-6] [PMID: 36071061]
[94]
Burgess, N.; Maguire, E.A.; O’Keefe, J. The human hippocampus and spatial and episodic memory. Neuron, 2002, 35(4), 625-641.
[http://dx.doi.org/10.1016/S0896-6273(02)00830-9] [PMID: 12194864]
[95]
Jourdain, P.; Bergersen, L.H.; Bhaukaurally, K.; Bezzi, P.; Santello, M.; Domercq, M.; Matute, C.; Tonello, F.; Gundersen, V.; Volterra, A. Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci., 2007, 10(3), 331-339.
[http://dx.doi.org/10.1038/nn1849] [PMID: 17310248]
[96]
Savtchouk, I.; Di Castro, M.A.; Ali, R.; Stubbe, H.; Luján, R.; Volterra, A. Circuit-specific control of the medial entorhinal inputs to the dentate gyrus by atypical presynaptic NMDARs activated by astrocytes. Proc. Natl. Acad. Sci., 2019, 116(27), 13602-13610.
[http://dx.doi.org/10.1073/pnas.1816013116] [PMID: 31152131]
[97]
Zhao, J.; Sun, J.; Zheng, Y.; Zheng, Y.; Shao, Y.; Li, Y.; Fei, F.; Xu, C.; Liu, X.; Wang, S.; Ruan, Y.; Liu, J.; Duan, S.; Chen, Z.; Wang, Y. Activated astrocytes attenuate neocortical seizures in rodent models through driving Na+-K+-ATPase. Nat. Commun., 2022, 13(1), 7136.
[http://dx.doi.org/10.1038/s41467-022-34662-2] [PMID: 36414629]
[98]
Kol, A.; Adamsky, A.; Groysman, M.; Kreisel, T.; London, M.; Goshen, I. Astrocytes contribute to remote memory formation by modulating hippocampal-cortical communication during learning. Nat. Neurosci., 2020, 23(10), 1229-1239.
[http://dx.doi.org/10.1038/s41593-020-0679-6] [PMID: 32747787]
[99]
Hasan, M.; Kanna, M.S.; Jun, W.; Ramkrishnan, A.S.; Iqbal, Z.; Lee, Y.; Li, Y. Schema‐like learning and memory consolidation acting through myelination. FASEB J., 2019, 33(11), 11758-11775.
[http://dx.doi.org/10.1096/fj.201900910R] [PMID: 31366238]
[100]
Liu, S.; Wong, H.Y.; Xie, L.; Iqbal, Z.; Lei, Z.; Fu, Z.; Lam, Y.Y.; Ramkrishnan, A.S.; Li, Y. Astrocytes in CA1 modulate schema establishment in the hippocampal-cortical neuron network. BMC Biol., 2022, 20(1), 250.
[http://dx.doi.org/10.1186/s12915-022-01445-6] [PMID: 36352395]
[101]
Lei, Z.; Xie, L.; Li, C.H.; Lam, Y.Y.; Ramkrishnan, A.S.; Fu, Z.; Zeng, X.; Liu, S.; Iqbal, Z.; Li, Y. Chemogenetic activation of astrocytes in the basolateral amygdala contributes to fear memory formation by modulating the amygdala-prefrontal cortex communication. Int. J. Mol. Sci., 2022, 23(11), 6092.
[http://dx.doi.org/10.3390/ijms23116092] [PMID: 35682767]
[102]
Doron, A.; Rubin, A.; Benmelech-Chovav, A.; Benaim, N.; Carmi, T.; Refaeli, R.; Novick, N.; Kreisel, T.; Ziv, Y.; Goshen, I. Hippocampal astrocytes encode reward location. Nature, 2022, 609(7928), 772-778.
[http://dx.doi.org/10.1038/s41586-022-05146-6] [PMID: 36045289]
[103]
Curreli, S.; Bonato, J.; Romanzi, S.; Panzeri, S.; Fellin, T. Complementary encoding of spatial information in hippocampal astrocytes. PLoS Biol., 2022, 20(3), e3001530.
[http://dx.doi.org/10.1371/journal.pbio.3001530] [PMID: 35239646]
[104]
Bellmund, J.L.S.; Gärdenfors, P.; Moser, E.I.; Doeller, C.F. Navigating cognition: Spatial codes for human thinking. Science, 2018, 362(6415), eaat6766.
[http://dx.doi.org/10.1126/science.aat6766] [PMID: 30409861]
[105]
Hartley, T.; Lever, C.; Burgess, N.; O’Keefe, J. Space in the brain: How the hippocampal formation supports spatial cognition. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369(1635), 20120510.
[http://dx.doi.org/10.1098/rstb.2012.0510] [PMID: 24366125]
[106]
Nagai, J.; Bellafard, A.; Qu, Z.; Yu, X.; Ollivier, M.; Gangwani, M.R.; Diaz-Castro, B.; Coppola, G.; Schumacher, S.M.; Golshani, P.; Gradinaru, V.; Khakh, B.S. Specific and behaviorally consequential astrocyte Gq GPCR signaling attenuation in vivo with iβARK. Neuron, 2021, 109(14), 2256-2274.e9.
[http://dx.doi.org/10.1016/j.neuron.2021.05.023] [PMID: 34139149]
[107]
Pannasch, U.; Vargová, L.; Reingruber, J.; Ezan, P.; Holcman, D.; Giaume, C.; Syková, E.; Rouach, N. Astroglial networks scale synaptic activity and plasticity. Proc. Natl. Acad. Sci., 2011, 108(20), 8467-8472.
[http://dx.doi.org/10.1073/pnas.1016650108] [PMID: 21536893]
[108]
Hösli, L.; Binini, N.; Ferrari, K.D.; Thieren, L.; Looser, Z.J.; Zuend, M.; Zanker, H.S.; Berry, S.; Holub, M.; Möbius, W.; Ruhwedel, T.; Nave, K.A.; Giaume, C.; Weber, B.; Saab, A.S. Decoupling astrocytes in adult mice impairs synaptic plasticity and spatial learning. Cell Rep., 2022, 38(10), 110484.
[http://dx.doi.org/10.1016/j.celrep.2022.110484] [PMID: 35263595]
[109]
Tao, X.D.; Liu, Z.R.; Zhang, Y.Q.; Zhang, X.H. Connexin43 hemichannels contribute to working memory and excitatory synaptic transmission of pyramidal neurons in the prefrontal cortex of rats. Life Sci., 2021, 286, 120049.
[http://dx.doi.org/10.1016/j.lfs.2021.120049] [PMID: 34662549]
[110]
Herzine, A.; Sekkat, G.; Kaminski, S.; Calcagno, G.; Boschi-Muller, S.; Safi, H.; Corbier, C.; Siest, S.; Claudepierre, T.; Yen, F.T. Lipolysis-stimulated lipoprotein receptor acts as sensor to regulate apoe release in astrocytes. Int. J. Mol. Sci., 2022, 23(15), 8630.
[http://dx.doi.org/10.3390/ijms23158630] [PMID: 35955777]
[111]
El Hajj, A.; Herzine, A.; Calcagno, G.; Désor, F.; Djelti, F.; Bombail, V.; Denis, I.; Oster, T.; Malaplate, C.; Vigier, M.; Kaminski, S.; Pauron, L.; Corbier, C.; Yen, F.T.; Lanhers, M.C.; Claudepierre, T. Targeted suppression of lipoprotein receptor LSR in astrocytes leads to olfactory and memory deficits in mice. Int. J. Mol. Sci., 2022, 23(4), 2049.
[http://dx.doi.org/10.3390/ijms23042049] [PMID: 35216163]
[112]
Baier, M.P.; Nagaraja, R.Y.; Yarbrough, H.P.; Owen, D.B.; Masingale, A.M.; Ranjit, R.; Stiles, M.A.; Murphy, A.; Agbaga, M.P.; Ahmad, M.; Sherry, D.M.; Kinter, M.T.; Van Remmen, H.; Logan, S. Selective ablation of Sod2 in astrocytes induces sex-specific effects on cognitive function, d-serine availability, and astrogliosis. J. Neurosci., 2022, 42(31), 5992-6006.
[http://dx.doi.org/10.1523/JNEUROSCI.2543-21.2022] [PMID: 35760531]
[113]
Curie, A.; Sacco, S.; Bussy, G.; de Saint Martin, A.; Boddaert, N.; Chanraud, S.; Meresse, I.; Chelly, J.; Zilbovicius, M.; des Portes, V. Impairment of cerebello-thalamo-frontal pathway in Rab-GDI mutated patients with pure mental deficiency. Eur. J. Med. Genet., 2009, 52(1), 6-13.
[http://dx.doi.org/10.1016/j.ejmg.2008.09.003] [PMID: 18992375]
[114]
Stenmark, H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol., 2009, 10(8), 513-525.
[http://dx.doi.org/10.1038/nrm2728] [PMID: 19603039]
[115]
D’Adamo, P.; Horvat, A.; Gurgone, A.; Mignogna, M.L.; Bianchi, V.; Masetti, M.; Ripamonti, M.; Taverna, S.; Velebit, J.; Malnar, M.; Muhič, M.; Fink, K.; Bachi, A.; Restuccia, U.; Belloli, S.; Moresco, R.M.; Mercalli, A.; Piemonti, L.; Potokar, M.; Bobnar, S.T.; Kreft, M.; Chowdhury, H.H.; Stenovec, M.; Vardjan, N.; Zorec, R. Inhibiting glycolysis rescues memory impairment in an intellectual disability Gdi1-null mouse. Metabolism, 2021, 116, 154463.
[http://dx.doi.org/10.1016/j.metabol.2020.154463] [PMID: 33309713]
[116]
Adamsky, A.; Kol, A.; Kreisel, T.; Doron, A.; Ozeri-Engelhard, N.; Melcer, T.; Refaeli, R.; Horn, H.; Regev, L.; Groysman, M.; London, M.; Goshen, I. Astrocytic activation generates de novo neuronal potentiation and memory enhancement. Cell, 2018, 174(1), 59-71.e14.
[http://dx.doi.org/10.1016/j.cell.2018.05.002] [PMID: 29804835]
[117]
Li, Y.; Li, L.; Wu, J.; Zhu, Z.; Feng, X.; Qin, L.; Zhu, Y.; Sun, L.; Liu, Y.; Qiu, Z.; Duan, S.; Yu, Y.Q. Activation of astrocytes in hippocampus decreases fear memory through adenosine A1 receptors. eLife, 2020, 9, e57155.
[http://dx.doi.org/10.7554/eLife.57155] [PMID: 32869747]
[118]
Fan, X.C.; Ma, C.N.; Song, J.C.; Liao, Z.H.; Huang, N.; Liu, X.; Ma, L. Rac1 signaling in amygdala astrocytes regulates fear memory acquisition and retrieval. Neurosci. Bull., 2021, 37(7), 947-958.
[http://dx.doi.org/10.1007/s12264-021-00677-w] [PMID: 33909243]
[119]
Li, W.P.; Su, X.H.; Hu, N.Y.; Hu, J.; Li, X.W.; Yang, J.M.; Gao, T.M. Astrocytes mediate cholinergic regulation of adult hippocampal neurogenesis and memory through M1 muscarinic receptor. Biol. Psychiatry, 2022, 92(12), 984-998.
[http://dx.doi.org/10.1016/j.biopsych.2022.04.019] [PMID: 35787318]
[120]
Badia-Soteras, A.; Heistek, T.S.; Kater, M.S.J.; Mak, A.; Negrean, A.; van den Oever, M.C.; Mansvelder, H.D.; Khakh, B.S.; Min, R.; Smit, A.B.; Verheijen, M.H.G. Retraction of astrocyte leaflets from the synapse enhances fear memory. Biol. Psychiatry, 2023, 94(3), 226-238.
[http://dx.doi.org/10.1016/j.biopsych.2022.10.013] [PMID: 36702661]
[121]
Zhang, K.; Förster, R.; He, W.; Liao, X.; Li, J.; Yang, C.; Qin, H.; Wang, M.; Ding, R.; Li, R.; Jian, T.; Wang, Y.; Zhang, J.; Yang, Z.; Jin, W.; Zhang, Y.; Qin, S.; Lu, Y.; Chen, T.; Stobart, J.; Weber, B.; Adelsberger, H.; Konnerth, A.; Chen, X. Fear learning induces α7-nicotinic acetylcholine receptor-mediated astrocytic responsiveness that is required for memory persistence. Nat. Neurosci., 2021, 24(12), 1686-1698.
[http://dx.doi.org/10.1038/s41593-021-00949-8] [PMID: 34782794]
[122]
Tertil, M.; Skupio, U.; Barut, J.; Dubovyk, V.; Wawrzczak-Bargiela, A.; Soltys, Z.; Golda, S.; Kudla, L.; Wiktorowska, L.; Szklarczyk, K.; Korostynski, M.; Przewlocki, R.; Slezak, M. Glucocorticoid receptor signaling in astrocytes is required for aversive memory formation. Transl. Psychiatry, 2018, 8(1), 255.
[http://dx.doi.org/10.1038/s41398-018-0300-x] [PMID: 30487639]
[123]
Iqbal, Z.; Liu, S.; Lei, Z.; Ramkrishnan, A.S.; Akter, M.; Li, Y. Astrocyte L-Lactate signaling in the acc regulates visceral pain aversive memory in rats. Cells, 2022, 12(1), 26.
[http://dx.doi.org/10.3390/cells12010026] [PMID: 36611820]
[124]
Iqbal, Z.; Lei, Z.; Ramkrishnan, A.S.; Liu, S.; Hasan, M.; Akter, M.; Lam, Y.Y.; Li, Y. Adrenergic signalling to astrocytes in anterior cingulate cortex contributes to pain-related aversive memory in rats. Commun. Biol., 2023, 6(1), 10.
[http://dx.doi.org/10.1038/s42003-022-04405-6] [PMID: 36604595]
[125]
Cheung, G.; Bataveljic, D.; Visser, J.; Kumar, N.; Moulard, J.; Dallérac, G.; Mozheiko, D.; Rollenhagen, A.; Ezan, P.; Mongin, C.; Chever, O.; Bemelmans, A.P.; Lübke, J.; Leray, I.; Rouach, N. Physiological synaptic activity and recognition memory require astroglial glutamine. Nat. Commun., 2022, 13(1), 753.
[http://dx.doi.org/10.1038/s41467-022-28331-7] [PMID: 35136061]
[126]
Ray, S.; Valekunja, U.K.; Stangherlin, A.; Howell, S.A.; Snijders, A.P.; Damodaran, G.; Reddy, A.B. Circadian rhythms in the absence of the clock gene Bmal1. Science, 2020, 367(6479), 800-806.
[http://dx.doi.org/10.1126/science.aaw7365] [PMID: 32054765]
[127]
Barca-Mayo, O.; Pons-Espinal, M.; Follert, P.; Armirotti, A.; Berdondini, L.; De Pietri Tonelli, D. Astrocyte deletion of Bmal1 alters daily locomotor activity and cognitive functions via GABA signalling. Nat. Commun., 2017, 8(1), 14336.
[http://dx.doi.org/10.1038/ncomms14336] [PMID: 28186121]
[128]
Sofroniew, M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci., 2009, 32(12), 638-647.
[http://dx.doi.org/10.1016/j.tins.2009.08.002] [PMID: 19782411]
[129]
Bellaver, B.; Souza, D.G.; Souza, D.O.; Quincozes-Santos, A. Hippocampal astrocyte cultures from adult and aged rats reproduce changes in glial functionality observed in the aging brain. Mol. Neurobiol., 2017, 54(4), 2969-2985.
[http://dx.doi.org/10.1007/s12035-016-9880-8] [PMID: 27026184]
[130]
Murphy-Royal, C.; Gordon, G.R.; Bains, J.S. Stress‐induced structural and functional modifications of astrocytes—Further implicating glia in the central response to stress. Glia, 2019, 67(10), 1806-1820.
[http://dx.doi.org/10.1002/glia.23610] [PMID: 30889320]
[131]
Tynan, R.J.; Beynon, S.B.; Hinwood, M.; Johnson, S.J.; Nilsson, M.; Woods, J.J.; Walker, F.R. Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol., 2013, 126(1), 75-91.
[http://dx.doi.org/10.1007/s00401-013-1102-0] [PMID: 23512378]
[132]
Jo, S.; Yarishkin, O.; Hwang, Y.J.; Chun, Y.E.; Park, M.; Woo, D.H.; Bae, J.Y.; Kim, T.; Lee, J.; Chun, H.; Park, H.J.; Lee, D.Y.; Hong, J.; Kim, H.Y.; Oh, S.J.; Park, S.J.; Lee, H.; Yoon, B.E.; Kim, Y.; Jeong, Y.; Shim, I.; Bae, Y.C.; Cho, J.; Kowall, N.W.; Ryu, H.; Hwang, E.; Kim, D.; Lee, C.J. GABA from reactive astrocytes impairs memory in mouse models of Alzheimer’s disease. Nat. Med., 2014, 20(8), 886-896.
[http://dx.doi.org/10.1038/nm.3639] [PMID: 24973918]
[133]
Chun, H.; Im, H.; Kang, Y.J.; Kim, Y.; Shin, J.H.; Won, W.; Lim, J.; Ju, Y.; Park, Y.M.; Kim, S.; Lee, S.E.; Lee, J.; Woo, J.; Hwang, Y.; Cho, H.; Jo, S.; Park, J.H.; Kim, D.; Kim, D.Y.; Seo, J.S.; Gwag, B.J.; Kim, Y.S.; Park, K.D.; Kaang, B.K.; Cho, H.; Ryu, H.; Lee, C.J. Severe reactive astrocytes precipitate pathological hallmarks of Alzheimer’s disease via H2O2− production. Nat. Neurosci., 2020, 23(12), 1555-1566.
[http://dx.doi.org/10.1038/s41593-020-00735-y] [PMID: 33199896]
[134]
Pereira, J.B.; Janelidze, S.; Smith, R.; Mattsson-Carlgren, N.; Palmqvist, S.; Teunissen, C.E.; Zetterberg, H.; Stomrud, E.; Ashton, N.J.; Blennow, K.; Hansson, O. Plasma GFAP is an early marker of amyloid-β but not tau pathology in Alzheimer’s disease. Brain, 2021, 144(11), 3505-3516.
[http://dx.doi.org/10.1093/brain/awab223] [PMID: 34259835]
[135]
Bettcher, B.M.; Olson, K.E.; Carlson, N.E.; McConnell, B.V.; Boyd, T.; Adame, V.; Solano, D.A.; Anton, P.; Markham, N.; Thaker, A.A.; Jensen, A.M.; Dallmann, E.N.; Potter, H.; Coughlan, C. Astrogliosis and episodic memory in late life: Higher GFAP is related to worse memory and white matter microstructure in healthy aging and Alzheimer’s disease. Neurobiol. Aging, 2021, 103, 68-77.
[http://dx.doi.org/10.1016/j.neurobiolaging.2021.02.012] [PMID: 33845398]
[136]
Iliff, J.J.; Wang, M.; Liao, Y.; Plogg, B.A.; Peng, W.; Gundersen, G.A.; Benveniste, H.; Vates, G.E.; Deane, R.; Goldman, S.A.; Nagelhus, E.A.; Nedergaard, M. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci. Transl. Med., 2012, 4(147), 147ra111.
[http://dx.doi.org/10.1126/scitranslmed.3003748] [PMID: 22896675]
[137]
Xu, Z.; Xiao, N.; Chen, Y.; Huang, H.; Marshall, C.; Gao, J.; Cai, Z.; Wu, T.; Hu, G.; Xiao, M. Deletion of aquaporin-4 in APP/PS1 mice exacerbates brain Aβ accumulation and memory deficits. Mol. Neurodegener., 2015, 10(1), 58.
[http://dx.doi.org/10.1186/s13024-015-0056-1] [PMID: 26526066]
[138]
Du, Z.; Song, Y.; Chen, X.; Zhang, W.; Zhang, G.; Li, H.; Chang, L.; Wu, Y. Knockdown of astrocytic Grin2a aggravates β‐amyloid‐induced memory and cognitive deficits through regulating nerve growth factor. Aging Cell, 2021, 20(8), e13437.
[http://dx.doi.org/10.1111/acel.13437] [PMID: 34291567]
[139]
Ju, Y.H.; Bhalla, M.; Hyeon, S.J.; Oh, J.E.; Yoo, S.; Chae, U.; Kwon, J.; Koh, W.; Lim, J.; Park, Y.M.; Lee, J.; Cho, I.J.; Lee, H.; Ryu, H.; Lee, C.J. Astrocytic urea cycle detoxifies Aβ-derived ammonia while impairing memory in Alzheimer’s disease. Cell Metab., 2022, 34(8), 1104-1120.e8.
[http://dx.doi.org/10.1016/j.cmet.2022.05.011] [PMID: 35738259]
[140]
Richetin, K.; Steullet, P.; Pachoud, M.; Perbet, R.; Parietti, E.; Maheswaran, M.; Eddarkaoui, S.; Bégard, S.; Pythoud, C.; Rey, M.; Caillierez, R.; Q Do, K.; Halliez, S.; Bezzi, P.; Buée, L.; Leuba, G.; Colin, M.; Toni, N.; Déglon, N. Tau accumulation in astrocytes of the dentate gyrus induces neuronal dysfunction and memory deficits in Alzheimer’s disease. Nat. Neurosci., 2020, 23(12), 1567-1579.
[http://dx.doi.org/10.1038/s41593-020-00728-x] [PMID: 33169029]
[141]
Holtzman, D.M.; Herz, J.; Bu, G. Apolipoprotein E and apolipoprotein E receptors: Normal biology and roles in Alzheimer disease. Cold Spring Harb. Perspect. Med., 2012, 2(3), a006312.
[http://dx.doi.org/10.1101/cshperspect.a006312] [PMID: 22393530]
[142]
Pitas, R.E.; Boyles, J.K.; Lee, S.H.; Foss, D.; Mahley, R.W. Astrocytes synthesize apolipoprotein E and metabolize apolipoprotein E-containing lipoproteins. Biochim. Biophys. Acta. Lipids Lipid Metab., 1987, 917(1), 148-161.
[http://dx.doi.org/10.1016/0005-2760(87)90295-5] [PMID: 3539206]
[143]
Montagne, A.; Nation, D.A.; Sagare, A.P.; Barisano, G.; Sweeney, M.D.; Chakhoyan, A.; Pachicano, M.; Joe, E.; Nelson, A.R.; D’Orazio, L.M.; Buennagel, D.P.; Harrington, M.G.; Benzinger, T.L.S.; Fagan, A.M.; Ringman, J.M.; Schneider, L.S.; Morris, J.C.; Reiman, E.M.; Caselli, R.J.; Chui, H.C.; Tcw, J.; Chen, Y.; Pa, J.; Conti, P.S.; Law, M.; Toga, A.W.; Zlokovic, B.V. APOE4 leads to blood–brain barrier dysfunction predicting cognitive decline. Nature, 2020, 581(7806), 71-76.
[http://dx.doi.org/10.1038/s41586-020-2247-3] [PMID: 32376954]
[144]
Sienski, G.; Narayan, P.; Bonner, J.M.; Kory, N.; Boland, S.; Arczewska, A.A.; Ralvenius, W.T.; Akay, L.; Lockshin, E.; He, L.; Milo, B.; Graziosi, A.; Baru, V.; Lewis, C.A.; Kellis, M.; Sabatini, D.M.; Tsai, L.H.; Lindquist, S. APOE4 disrupts intracellular lipid homeostasis in human iPSC-derived glia. Sci. Transl. Med., 2021, 13(583), eaaz4564.
[http://dx.doi.org/10.1126/scitranslmed.aaz4564] [PMID: 33658354]
[145]
Saroja, S.R.; Gorbachev, K.; Julia, T.C.W.; Goate, A.M.; Pereira, A.C. Astrocyte-secreted glypican-4 drives APOE4-dependent tau hyperphosphorylation. Proc. Natl. Acad. Sci., 2022, 119(34), e2108870119.
[http://dx.doi.org/10.1073/pnas.2108870119] [PMID: 35969759]
[146]
Tcw, J.; Qian, L.; Pipalia, N.H.; Chao, M.J.; Liang, S.A.; Shi, Y.; Jain, B.R.; Bertelsen, S.E.; Kapoor, M.; Marcora, E.; Sikora, E.; Andrews, E.J.; Martini, A.C.; Karch, C.M.; Head, E.; Holtzman, D.M.; Zhang, B.; Wang, M.; Maxfield, F.R.; Poon, W.W.; Goate, A.M. Cholesterol and matrisome pathways dysregulated in astrocytes and microglia. Cell, 2022, 185(13), 2213-2233.e25.
[http://dx.doi.org/10.1016/j.cell.2022.05.017] [PMID: 35750033]
[147]
Wang, C.; Xiong, M.; Gratuze, M.; Bao, X.; Shi, Y.; Andhey, P.S.; Manis, M.; Schroeder, C.; Yin, Z.; Madore, C.; Butovsky, O.; Artyomov, M.; Ulrich, J.D.; Holtzman, D.M. Selective removal of astrocytic APOE4 strongly protects against tau-mediated neurodegeneration and decreases synaptic phagocytosis by microglia. Neuron, 2021, 109(10), 1657-1674.
[http://dx.doi.org/10.1016/j.neuron.2021.03.024]
[148]
Le Douce, J.; Maugard, M.; Veran, J.; Matos, M.; Jégo, P.; Vigneron, P.A.; Faivre, E.; Toussay, X.; Vandenberghe, M.; Balbastre, Y.; Piquet, J.; Guiot, E.; Tran, N.T.; Taverna, M.; Marinesco, S.; Koyanagi, A.; Furuya, S.; Gaudin-Guérif, M.; Goutal, S.; Ghettas, A.; Pruvost, A.; Bemelmans, A.P.; Gaillard, M.C.; Cambon, K.; Stimmer, L.; Sazdovitch, V.; Duyckaerts, C.; Knott, G.; Hérard, A.S.; Delzescaux, T.; Hantraye, P.; Brouillet, E.; Cauli, B.; Oliet, S.H.R.; Panatier, A.; Bonvento, G. Impairment of glycolysis-derived l-serine production in astrocytes contributes to cognitive deficits in alzheimer’s disease. Cell Metab., 2020, 31(3), 503-517.e8.
[http://dx.doi.org/10.1016/j.cmet.2020.02.004] [PMID: 32130882]
[149]
Bosson, A.; Paumier, A.; Boisseau, S.; Jacquier-Sarlin, M.; Buisson, A.; Albrieux, M. TRPA1 channels promote astrocytic Ca2+ hyperactivity and synaptic dysfunction mediated by oligomeric forms of amyloid-β peptide. Mol. Neurodegener., 2017, 12(1), 53.
[http://dx.doi.org/10.1186/s13024-017-0194-8] [PMID: 28683776]
[150]
Paumier, A.; Boisseau, S.; Jacquier-Sarlin, M.; Pernet-Gallay, K.; Buisson, A.; Albrieux, M. Astrocyte–neuron interplay is critical for Alzheimer’s disease pathogenesis and is rescued by TRPA1 channel blockade. Brain, 2022, 145(1), 388-405.
[http://dx.doi.org/10.1093/brain/awab281] [PMID: 34302466]
[151]
Lia, A.; Sansevero, G.; Chiavegato, A.; Sbrissa, M.; Pendin, D.; Mariotti, L.; Pozzan, T.; Berardi, N.; Carmignoto, G.; Fasolato, C.; Zonta, M. Rescue of astrocyte activity by the calcium sensor STIM1 restores long-term synaptic plasticity in female mice modelling Alzheimer’s disease. Nat. Commun., 2023, 14(1), 1590.
[http://dx.doi.org/10.1038/s41467-023-37240-2] [PMID: 36949142]
[152]
Reichenbach, N.; Delekate, A.; Breithausen, B.; Keppler, K.; Poll, S.; Schulte, T.; Peter, J.; Plescher, M.; Hansen, J.N.; Blank, N.; Keller, A.; Fuhrmann, M.; Henneberger, C.; Halle, A.; Petzold, G.C. P2Y1 receptor blockade normalizes network dysfunction and cognition in an Alzheimer’s disease model. J. Exp. Med., 2018, 215(6), 1649-1663.
[http://dx.doi.org/10.1084/jem.20171487] [PMID: 29724785]
[153]
Raha, S.; Ghosh, A.; Dutta, D.; Patel, D.R.; Pahan, K. Activation of PPARα enhances astroglial uptake and degradation of β-amyloid. Sci. Signal., 2021, 14(706), eabg4747.
[http://dx.doi.org/10.1126/scisignal.abg4747] [PMID: 34699252]
[154]
McAlpine, C.S.; Park, J.; Griciuc, A.; Kim, E.; Choi, S.H.; Iwamoto, Y.; Kiss, M.G.; Christie, K.A.; Vinegoni, C.; Poller, W.C.; Mindur, J.E.; Chan, C.T.; He, S.; Janssen, H.; Wong, L.P.; Downey, J.; Singh, S.; Anzai, A.; Kahles, F.; Jorfi, M.; Feruglio, P.F.; Sadreyev, R.I.; Weissleder, R.; Kleinstiver, B.P.; Nahrendorf, M.; Tanzi, R.E.; Swirski, F.K. Astrocytic interleukin-3 programs microglia and limits Alzheimer’s disease. Nature, 2021, 595(7869), 701-706.
[http://dx.doi.org/10.1038/s41586-021-03734-6] [PMID: 34262178]
[155]
Jiwaji, Z.; Tiwari, S.S.; Avilés-Reyes, R.X.; Hooley, M.; Hampton, D.; Torvell, M.; Johnson, D.A.; McQueen, J.; Baxter, P.; Sabari-Sankar, K.; Qiu, J.; He, X.; Fowler, J.; Febery, J.; Gregory, J.; Rose, J.; Tulloch, J.; Loan, J.; Story, D.; McDade, K.; Smith, A.M.; Greer, P.; Ball, M.; Kind, P.C.; Matthews, P.M.; Smith, C.; Dando, O.; Spires-Jones, T.L.; Johnson, J.A.; Chandran, S.; Hardingham, G.E. Reactive astrocytes acquire neuroprotective as well as deleterious signatures in response to Tau and Aß pathology. Nat. Commun., 2022, 13(1), 135.
[http://dx.doi.org/10.1038/s41467-021-27702-w] [PMID: 35013236]
[156]
Popov, A.; Brazhe, A.; Denisov, P.; Sutyagina, O.; Li, L.; Lazareva, N.; Verkhratsky, A.; Semyanov, A. Astrocyte dystrophy in ageing brain parallels impaired synaptic plasticity. Aging Cell, 2021, 20(3), e13334.
[http://dx.doi.org/10.1111/acel.13334] [PMID: 33675569]
[157]
Verkhratsky, A.; Augusto-Oliveira, M.; Pivoriūnas, A.; Popov, A.; Brazhe, A.; Semyanov, A. Astroglial asthenia and loss of function, rather than reactivity, contribute to the ageing of the brain. Pflugers Arch., 2021, 473(5), 753-774.
[http://dx.doi.org/10.1007/s00424-020-02465-3] [PMID: 32979108]
[158]
Ding, F.; Liang, S.; Li, R.; Yang, Z.; He, Y.; Yang, S.; Duan, Q.; Zhang, J.; Lyu, J.; Zhou, Z.; Huang, M.; Wang, H.; Li, J.; Yang, C.; Wang, Y.; Gong, M.; Chen, S.; Jia, H.; Chen, X.; Liao, X.; Fu, L.; Zhang, K. Astrocytes exhibit diverse Ca2+ changes at subcellular domains during brain aging. Front. Aging Neurosci., 2022, 14, 1029533.
[http://dx.doi.org/10.3389/fnagi.2022.1029533] [PMID: 36389078]
[159]
Soreq, L.; Rose, J.; Soreq, E.; Hardy, J.; Trabzuni, D.; Cookson, M.R.; Smith, C.; Ryten, M.; Patani, R.; Ule, J. Major shifts in glial regional identity are a transcriptional hallmark of human brain aging. Cell Rep., 2017, 18(2), 557-570.
[http://dx.doi.org/10.1016/j.celrep.2016.12.011] [PMID: 28076797]
[160]
Clarke, L.E.; Liddelow, S.A.; Chakraborty, C.; Münch, A.E.; Heiman, M.; Barres, B.A. Normal aging induces A1-like astrocyte reactivity. Proc. Natl. Acad. Sci., 2018, 115(8), E1896-E1905.
[http://dx.doi.org/10.1073/pnas.1800165115] [PMID: 29437957]
[161]
Allen, W.E.; Blosser, T.R.; Sullivan, Z.A.; Dulac, C.; Zhuang, X. Molecular and spatial signatures of mouse brain aging at single-cell resolution. Cell, 2023, 186(1), 194-208.e18.
[http://dx.doi.org/10.1016/j.cell.2022.12.010] [PMID: 36580914]
[162]
Preininger, M.K.; Kaufer, D. Blood-brain barrier dysfunction and astrocyte senescence as reciprocal drivers of neuropathology in aging. Int. J. Mol. Sci., 2022, 23(11), 6217.
[http://dx.doi.org/10.3390/ijms23116217] [PMID: 35682895]
[163]
Cohen, J.; Torres, C. Astrocyte senescence: Evidence and significance. Aging Cell, 2019, 18(3), e12937.
[http://dx.doi.org/10.1111/acel.12937] [PMID: 30815970]
[164]
Boisvert, M.M.; Erikson, G.A.; Shokhirev, M.N.; Allen, N.J. The aging astrocyte transcriptome from multiple regions of the mouse brain. Cell Rep., 2018, 22(1), 269-285.
[http://dx.doi.org/10.1016/j.celrep.2017.12.039] [PMID: 29298427]
[165]
Orre, M.; Kamphuis, W.; Osborn, L.M.; Melief, J.; Kooijman, L.; Huitinga, I.; Klooster, J.; Bossers, K.; Hol, E.M. Acute isolation and transcriptome characterization of cortical astrocytes and microglia from young and aged mice. Neurobiol. Aging, 2014, 35(1), 1-14.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.07.008] [PMID: 23954174]
[166]
Boender, A.J.; Bontempi, L.; Nava, L.; Pelloux, Y.; Tonini, R. Striatal astrocytes shape behavioral flexibility via regulation of the glutamate transporter EAAT2. Biol. Psychiatry, 2021, 89(11), 1045-1057.
[http://dx.doi.org/10.1016/j.biopsych.2020.11.015] [PMID: 33516457]
[167]
Sharma, A.; Kazim, S.F.; Larson, C.S.; Ramakrishnan, A.; Gray, J.D.; McEwen, B.S.; Rosenberg, P.A.; Shen, L.; Pereira, A.C. Divergent roles of astrocytic versus neuronal EAAT2 deficiency on cognition and overlap with aging and Alzheimer’s molecular signatures. Proc. Natl. Acad. Sci., 2019, 116(43), 21800-21811.
[http://dx.doi.org/10.1073/pnas.1903566116] [PMID: 31591195]
[168]
Yang, Z.; Gong, M.; Jian, T.; Li, J.; Yang, C.; Ma, Q.; Deng, P.; Wang, Y.; Huang, M.; Wang, H.; Yang, S.; Chen, X.; Yu, Z.; Wang, M.; Chen, C.; Zhang, K. Engrafted glial progenitor cells yield long-term integration and sensory improvement in aged mice. Stem Cell Res. Ther., 2022, 13(1), 285.
[http://dx.doi.org/10.1186/s13287-022-02959-0] [PMID: 35765112]
[169]
Xu, X.; Shen, X.; Wang, J.; Feng, W.; Wang, M.; Miao, X.; Wu, Q.; Wu, L.; Wang, X.; Ma, Y.; Wu, S.; Bao, X.; Wang, W.; Wang, Y.; Huang, Z. YAP prevents premature senescence of astrocytes and cognitive decline of Alzheimer’s disease through regulating CDK6 signaling. Aging Cell, 2021, 20(9), e13465.
[http://dx.doi.org/10.1111/acel.13465] [PMID: 34415667]
[170]
Raihan, O.; Brishti, A.; Molla, M.R.; Li, W.; Zhang, Q.; Xu, P.; Khan, M.I.; Zhang, J.; Liu, Q. The age-dependent elevation of miR-335-3p leads to reduced cholesterol and impaired memory in brain. Neuroscience, 2018, 390, 160-173.
[http://dx.doi.org/10.1016/j.neuroscience.2018.08.003] [PMID: 30125687]
[171]
Patel, B.N.; Dunn, R.J.; Jeong, S.Y.; Zhu, Q.; Julien, J.P.; David, S. Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury. J. Neurosci., 2002, 22(15), 6578-6586.
[http://dx.doi.org/10.1523/JNEUROSCI.22-15-06578.2002] [PMID: 12151537]
[172]
Li, Z.D.; Li, H.; Kang, S.; Cui, Y.G.; Zheng, H.; Wang, P.; Han, K.; Yu, P.; Chang, Y.Z. The divergent effects of astrocyte ceruloplasmin on learning and memory function in young and old mice. Cell Death Dis., 2022, 13(11), 1006.
[http://dx.doi.org/10.1038/s41419-022-05459-4] [PMID: 36443285]
[173]
Han, F.; Xiao, B.; Wen, L. Loss of glial cells of the hippocampus in a rat model of post-traumatic stress disorder. Neurochem. Res., 2015, 40(5), 942-951.
[http://dx.doi.org/10.1007/s11064-015-1549-6] [PMID: 25749890]
[174]
Imbe, H.; Kimura, A.; Donishi, T.; Kaneoke, Y. Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter. Neuroscience, 2012, 223, 209-218.
[http://dx.doi.org/10.1016/j.neuroscience.2012.08.007] [PMID: 22890077]
[175]
Saur, L.; Baptista, P.P.A.; Bagatini, P.B.; Neves, L.T.; de Oliveira, R.M.; Vaz, S.P.; Ferreira, K.; Machado, S.A.; Mestriner, R.G.; Xavier, L.L. Experimental post-traumatic stress disorder decreases astrocyte density and changes astrocytic polarity in the CA1 hippocampus of male rats. Neurochem. Res., 2016, 41(4), 892-904.
[http://dx.doi.org/10.1007/s11064-015-1770-3] [PMID: 26577396]
[176]
Wang, J.; Gao, F.; Cui, S.; Yang, S.; Gao, F.; Wang, X.; Zhu, G. Utility of 7,8-dihydroxyflavone in preventing astrocytic and synaptic deficits in the hippocampus elicited by PTSD. Pharmacol. Res., 2022, 176, 106079.
[http://dx.doi.org/10.1016/j.phrs.2022.106079] [PMID: 35026406]
[177]
Kitayama, N.; Vaccarino, V.; Kutner, M.; Weiss, P.; Bremner, J.D. Magnetic resonance imaging (MRI) measurement of hippocampal volume in posttraumatic stress disorder: A meta-analysis. J. Affect. Disord., 2005, 88(1), 79-86.
[http://dx.doi.org/10.1016/j.jad.2005.05.014] [PMID: 16033700]
[178]
Gilbertson, M.W.; Shenton, M.E.; Ciszewski, A.; Kasai, K.; Lasko, N.B.; Orr, S.P.; Pitman, R.K. Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat. Neurosci., 2002, 5(11), 1242-1247.
[http://dx.doi.org/10.1038/nn958] [PMID: 12379862]
[179]
Perez-Urrutia, N.; Mendoza, C.; Alvarez-Ricartes, N.; Oliveros-Matus, P.; Echeverria, F.; Grizzell, J.A.; Barreto, G.E.; Iarkov, A.; Echeverria, V. Intranasal cotinine improves memory, and reduces depressive-like behavior, and GFAP + cells loss induced by restraint stress in mice. Exp. Neurol., 2017, 295, 211-221.
[http://dx.doi.org/10.1016/j.expneurol.2017.06.016] [PMID: 28625590]
[180]
Wingo, T.S.; Gerasimov, E.S.; Liu, Y.; Duong, D.M.; Vattathil, S.M.; Lori, A.; Gockley, J.; Breen, M.S.; Maihofer, A.X.; Nievergelt, C.M.; Koenen, K.C.; Levey, D.F.; Gelernter, J.; Stein, M.B.; Ressler, K.J.; Bennett, D.A.; Levey, A.I.; Seyfried, N.T.; Wingo, A.P. Integrating human brain proteomes with genome-wide association data implicates novel proteins in post-traumatic stress disorder. Mol. Psychiatry, 2022, 27(7), 3075-3084.
[http://dx.doi.org/10.1038/s41380-022-01544-4] [PMID: 35449297]
[181]
Gao, F.; Wang, J.; Yang, S.; Ji, M.; Zhu, G. Fear extinction induced by activation of PKA ameliorates anxiety-like behavior in PTSD mice. Neuropharmacology, 2023, 222, 109306.
[http://dx.doi.org/10.1016/j.neuropharm.2022.109306] [PMID: 36341808]
[182]
Ji, M.; Zhang, Z.; Gao, F.; Yang, S.; Wang, J.; Wang, X.; Zhu, G. Curculigoside rescues hippocampal synaptic deficits elicited by PTSD through activating CAMP‐PKA signaling. Phytother. Res., 2023, 37(2), 759-773.
[http://dx.doi.org/10.1002/ptr.7658] [PMID: 36200803]
[183]
Yang, S.; Qu, Y.; Wang, J.; Gao, F.; Ji, M.; Xie, P.; Zhu, A.; Tan, B.; Wang, X.; Zhu, G. Anshen Dingzhi prescription in the treatment of PTSD in mice: Investigation of the underlying mechanism from the perspective of hippocampal synaptic function. Phytomedicine, 2022, 101, 154139.
[http://dx.doi.org/10.1016/j.phymed.2022.154139] [PMID: 35523115]
[184]
Oliveros-Matus, P.; Perez-Urrutia, N.; Alvarez-Ricartes, N.; Echeverria, F.; Barreto, G.E.; Elliott, J.; Iarkov, A.; Echeverria, V. Cotinine enhances fear extinction and astrocyte survival by mechanisms involving the nicotinic acetylcholine receptors signaling. Front. Pharmacol., 2020, 11, 303.
[http://dx.doi.org/10.3389/fphar.2020.00303] [PMID: 32300297]
[185]
Ohno, Y. Astrocytic Kir4.1 potassium channels as a novel therapeutic target for epilepsy and mood disorders. Neural Regen. Res., 2018, 13(4), 651-652.
[http://dx.doi.org/10.4103/1673-5374.230355] [PMID: 29722316]
[186]
Tong, X.; Ao, Y.; Faas, G.C.; Nwaobi, S.E.; Xu, J.; Haustein, M.D.; Anderson, M.A.; Mody, I.; Olsen, M.L.; Sofroniew, M.V.; Khakh, B.S. Astrocyte Kir4.1 ion channel deficits contribute to neuronal dysfunction in Huntington’s disease model mice. Nat. Neurosci., 2014, 17(5), 694-703.
[http://dx.doi.org/10.1038/nn.3691] [PMID: 24686787]
[187]
Zhang, Z.; Song, Z.; Shen, F.; Xie, P.; Wang, J.; Zhu, A.; Zhu, G. Ginsenoside Rg1 prevents PTSD-like behaviors in mice through promoting synaptic proteins, reducing kir4.1 and TNF-α in the hippocampus. Mol. Neurobiol., 2021, 58(4), 1550-1563.
[http://dx.doi.org/10.1007/s12035-020-02213-9] [PMID: 33215390]
[188]
Zhao, M.; Li, D.; Shimazu, K.; Zhou, Y.X.; Lu, B.; Deng, C.X. Fibroblast growth factor receptor-1 is required for long-term potentiation, memory consolidation, and neurogenesis. Biol. Psychiatry, 2007, 62(5), 381-390.
[http://dx.doi.org/10.1016/j.biopsych.2006.10.019] [PMID: 17239352]
[189]
Xia, L.; Zhai, M.; Wang, L.; Miao, D.; Zhu, X.; Wang, W. FGF2 blocks PTSD symptoms via an astrocyte-based mechanism. Behav. Brain Res., 2013, 256, 472-480.
[http://dx.doi.org/10.1016/j.bbr.2013.08.048] [PMID: 24013012]
[190]
Feng, D.; Guo, B.; Liu, G.; Wang, B.; Wang, W.; Gao, G.; Qin, H.; Wu, S. FGF2 alleviates PTSD symptoms in rats by restoring GLAST function in astrocytes via the JAK/STAT pathway. Eur. Neuropsychopharmacol., 2015, 25(8), 1287-1299.
[http://dx.doi.org/10.1016/j.euroneuro.2015.04.020] [PMID: 25979764]
[191]
Wang, J.; Holt, L.M.; Huang, H.H.; Sesack, S.R.; Nestler, E.J.; Dong, Y. Astrocytes in cocaine addiction and beyond. Mol. Psychiatry, 2022, 27(1), 652-668.
[http://dx.doi.org/10.1038/s41380-021-01080-7] [PMID: 33837268]
[192]
Ma, R.; Kutchy, N.A.; Hu, G. Astrocyte-derived extracellular vesicle-mediated activation of primary ciliary signaling contributes to the development of morphine tolerance. Biol. Psychiatry, 2021, 90(8), 575-585.
[http://dx.doi.org/10.1016/j.biopsych.2021.06.009] [PMID: 34417054]
[193]
Canedo, T.; Portugal, C.C.; Socodato, R.; Almeida, T.O.; Terceiro, A.F.; Bravo, J.; Silva, A.I.; Magalhães, J.D.; Guerra-Gomes, S.; Oliveira, J.F.; Sousa, N.; Magalhães, A.; Relvas, J.B.; Summavielle, T. Astrocyte-derived TNF and glutamate critically modulate microglia activation by methamphetamine. Neuropsychopharmacology, 2021, 46(13), 2358-2370.
[http://dx.doi.org/10.1038/s41386-021-01139-7] [PMID: 34400780]
[194]
Jouroukhin, Y.; Zhu, X.; Shevelkin, A.V.; Hasegawa, Y.; Abazyan, B.; Saito, A.; Pevsner, J.; Kamiya, A.; Pletnikov, M.V. Adolescent Δ9-tetrahydrocannabinol exposure and astrocyte-specific genetic vulnerability converge on nuclear factor-κB–cyclooxygenase-2 signaling to impair memory in adulthood. Biol. Psychiatry, 2019, 85(11), 891-903.
[http://dx.doi.org/10.1016/j.biopsych.2018.07.024] [PMID: 30219209]
[195]
Shelkar, G.P.; Gandhi, P.J.; Liu, J.; Dravid, S.M. Cocaine preference and neuroadaptations are maintained by astrocytic NMDA receptors in the nucleus accumbens. Sci. Adv., 2022, 8(29), eabo6574.
[http://dx.doi.org/10.1126/sciadv.abo6574] [PMID: 35867797]
[196]
Boury-Jamot, B.; Carrard, A.; Martin, J.L.; Halfon, O.; Magistretti, P.J.; Boutrel, B. Disrupting astrocyte–neuron lactate transfer persistently reduces conditioned responses to cocaine. Mol. Psychiatry, 2016, 21(8), 1070-1076.
[http://dx.doi.org/10.1038/mp.2015.157] [PMID: 26503760]
[197]
Shi, P.; Li, Z.; He, T.; Li, N.; Xu, X.; Yu, P.; Lu, X.; Nie, J.; Liu, D.; Cai, Q.; Guan, Y.; Ge, F.; Wang, J.; Guan, X. Astrocyte‐selective STAT3 knockdown rescues methamphetamine withdrawal‐disrupted spatial memory in mice via restoring the astrocytic capacity of glutamate clearance in DCA1. Glia, 2021, 69(10), 2404-2418.
[http://dx.doi.org/10.1002/glia.24046] [PMID: 34110044]
[198]
Molofsky, A.V.; Kelley, K.W.; Tsai, H.H.; Redmond, S.A.; Chang, S.M.; Madireddy, L.; Chan, J.R.; Baranzini, S.E.; Ullian, E.M.; Rowitch, D.H. Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature, 2014, 509(7499), 189-194.
[http://dx.doi.org/10.1038/nature13161] [PMID: 24776795]
[199]
Blanco-Suarez, E.; Liu, T.F.; Kopelevich, A.; Allen, N.J. Astrocyte-secreted chordin-like 1 drives synapse maturation and limits plasticity by increasing synaptic glua2 ampa receptors. Neuron, 2018, 100(5), 1116-1132.e13.
[http://dx.doi.org/10.1016/j.neuron.2018.09.043] [PMID: 30344043]
[200]
Nazari, S.; Amiri, M.; Faez, K.; Van Hulle, M.M. Information transmitted from bioinspired neuron–astrocyte network improves cortical spiking network’s pattern recognition performance. IEEE Trans. Neural Netw. Learn. Syst., 2020, 31(2), 464-474.
[http://dx.doi.org/10.1109/TNNLS.2019.2905003] [PMID: 30990195]
[201]
De Pittà, M.; Brunel, N. Multiple forms of working memory emerge from synapse–astrocyte interactions in a neuron–glia network model. Proc. Natl. Acad. Sci., 2022, 119(43), e2207912119.
[http://dx.doi.org/10.1073/pnas.2207912119] [PMID: 36256810]
[202]
Becker, S.; Nold, A.; Tchumatchenko, T. Modulation of working memory duration by synaptic and astrocytic mechanisms. PLOS Comput. Biol., 2022, 18(10), e1010543.
[http://dx.doi.org/10.1371/journal.pcbi.1010543] [PMID: 36191056]
[203]
Verdera, H.C.; Kuranda, K.; Mingozzi, F. AAV vector immunogenicity in humans: A long journey to successful gene transfer. Mol. Ther., 2020, 28(3), 723-746.
[http://dx.doi.org/10.1016/j.ymthe.2019.12.010] [PMID: 31972133]
[204]
Wang, Q.; Li, W.; Lei, W.; Chen, G.; Xiang, Z.; Xu, L.; Liu, M. Lineage tracing of direct astrocyte-to-neuron conversion in the mouse cortex. Neural Regen. Res., 2021, 16(4), 750-756.
[http://dx.doi.org/10.4103/1673-5374.295925] [PMID: 33063738]
[205]
Zhang, Y.; Li, B.; Cananzi, S.; Han, C.; Wang, L.L.; Zou, Y.; Fu, Y.X.; Hon, G.C.; Zhang, C.L. A single factor elicits multilineage reprogramming of astrocytes in the adult mouse striatum. Proc. Natl. Acad. Sci., 2022, 119(11), e2107339119.
[http://dx.doi.org/10.1073/pnas.2107339119] [PMID: 35254903]
[206]
Guo, Z.; Zhang, L.; Wu, Z.; Chen, Y.; Wang, F.; Chen, G. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer’s disease model. Cell Stem Cell, 2014, 14(2), 188-202.
[http://dx.doi.org/10.1016/j.stem.2013.12.001] [PMID: 24360883]

Rights & Permissions Print Cite
© 2025 Bentham Science Publishers | Privacy Policy