Molecular mechanisms of astrocyte involvement in synaptogenesis and brain synaptic plasticity

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Abstract

Astrocytes perform a wide range of important functions in the brain. As structural and functional components of synapses, astrocytes secrete various factors (proteins, lipids, small molecules, etc.) that bind to neuronal receptor and contribute to synaptogenesis and regulation of synaptic contacts. Astrocytic factors play a key role in the formation of neural networks undergoing short- and long-term synaptic morphological and functional rearrangements essential in the memory formation and behavior. The review summarizes the data on the molecular mechanisms mediating the involvement of astrocyte-secreted factors in synaptogenesis in the brain and provides up-to-date information on the role of astrocytes and astrocytic synaptogenic factors in the long-term plastic rearrangements of synaptic contacts.

About the authors

L. G Khaspekov

Research Center of Neurology

Email: khaspekleon@mail.ru
125367 Moscow, Russia

L. E Frumkina

Research Center of Neurology

Email: khaspekleon@mail.ru
125367 Moscow, Russia

References

  1. Abbink, M. R., van Deijk, A. F., Heine, V. M., Verheijen, M. H., and Korosi, A. (2019) The involvement of astrocytes in early-life adversity induced programming of the brain, Glia, 67, 1637-1653, doi: 10.1002/glia.23625.
  2. Perez-Catalan, N. A., Doe, C. Q., and Ackerman, S. D. (2021) The role of astrocyte-mediated plasticity in neural circuit development and function, Neural Dev., 16, 1, doi: 10.1186/s13064-020-00151-9.
  3. Aleksandrova, M. A., and Sukhinich, K. K. (2022) Astrocytes of the brain: retinue plays the king, Russ. J. Dev. Biol., 53, 252-271, doi: 10.1134/S1062360422040026.
  4. Fossati, G., Matteoli, M., and Menna, E. (2020) Astrocytic factors controlling synaptogenesis: a team play, Cells, 9, 2173, doi: 10.3390/cells9102173.
  5. Bayraktar, O. A., Fuentealba, L. C., Alvarez-Buylla, A., and Rowitch, D. H. (2015) Astrocyte development and heterogeneity, Cold Spring Harb. Perspect. Biol., 7, a020362, doi: 10.1101/cshperspect.a020362.
  6. Buosi, A. S., Matias, I., Araujo, A. P. B., Batista, C., and Gomes, F. C. A. (2018) Heterogeneity in synaptogenic profile of astrocytes from different brain regions, Mol. Neurobiol., 55, 751-762, doi: 10.1007/s12035-016-0343-z.
  7. Baldwin, K. T., and Eroglu, C. (2017) Molecular mechanisms of astrocyte-induced synaptogenesis, Curr. Opin. Neurobiol., 45, 113-120, doi: 10.1016/j.conb.2017.05.006.
  8. Qi, C., Luo, L. D., Feng, I., and Ma, S. (2022) Molecular mechanisms of synaptogenesis, Front. Synaptic Neurosci., 14, 939793, doi: 10.3389/fnsyn.2022.939793.
  9. Durkee, C. A., and Araque, A. (2019) Diversity and specificity of astrocyte-neuron communication, Neuroscience, 396, 73-78, doi: 10.1016/j.neuroscience.2018.11.010.
  10. Hasan, U., and Singh, S. K. (2019) The astrocyte-neuron interface: An overview on molecular and cellular dynamics controlling formation and maintenance of the tripartite synapse, Methods Mol. Biol., 1938, 3-18, doi: 10.1007/978-1-4939-9068-9_1.
  11. Meyer-Franke, A., Kaplan, M. R., Pfrieger, F. W., and Barres, B. A. (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture, Neuron, 15, 805-819, doi: 10.1016/0896-6273(95)90172-8.
  12. Nägler, K., Mauch, D. H., and Pfrieger, F. W. (2001) Glia-derived signals induce synapse formation in neurones of the rat central nervous system, J. Physiol., 533, 665-679, doi: 10.1111/j.1469-7793.2001.00665.x.
  13. Pfrieger, F. W., and Barres, B. A. (1997) Synaptic efficacy enhanced by glial cells in vitro, Science, 277, 1684-1687, doi: 10.1126/science.277.5332.1684.
  14. Johnson, M. A., Weick, J. P., Pearce, R. A., and Zhang, S. C. (2007) Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture, J. Neurosci., 27, 3069-3077, doi: 10.1523/JNEUROSCI.4562-06.2007.
  15. Farhy-Tselnicker, I., and Allen, N. J. (2018) Astrocytes, neurons, synapses: a tripartite view on cortical circuit development, Neural Dev., 13, 7, doi: 10.1186/s13064-018-0104-y.
  16. Saint-Martin, M., and Goda, Y. (2022) Astrocyte-synapse interactions and cell adhesion molecules, FEBS J., doi: 10.1111/febs.16540.
  17. Tan, C. X., and Eroglu, C. (2021) Cell adhesion molecules regulating astrocyte-neuron interactions, Curr. Opin. Neurobiol., 69, 170-177, doi: 10.1016/j.conb.2021.03.015.
  18. Augusto-Oliveira, M., Arrifa, A., and Crespo-Lopez, M. E. (2020) Astroglia-specific contributions to the regulation of synapses, cognition and behavior, Neurosci. Biobehav. Rev., 118, 331-357, doi: 10.1016/j.neubiorev.2020.07.039.
  19. Hughes, E. G., Elmariah, S. B., and Balice-Gordon, R. J. (2010) Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis, Mol. Cell. Neurosci., 43, 136-145, doi: 10.1016/j.mcn.2009.10.004.
  20. Shan, L., Zhang, T., Fan, K., Cai, W., and Liu, H. (2021) Astrocyte-neuron signaling in synaptogenesis, Front. Cell. Dev. Biol., 9, 680301, doi: 10.3389/fcell.2021.680301.
  21. Adams, J. C. (2001) Thrombospondins: multifunctional regulators of cell interactions, Annu. Rev. Cell Dev. Biol., 17, 25-51, doi: 10.1146/annurev.cellbio.17.1.25.
  22. Christopherson, K. S., Ullian, E. M., Stokes, C. C., Mullowney, C. E., Hell, J. W., Agah, A., Lawler, J., Mosher, D. F., Bornstein, P., and Barres, B. A. (2005) Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis, Cell, 120, 421-433, doi: 10.1016/j.cell.2004.12.020.
  23. Risher, W. C., and Eroglu, C. (2012) Thrombospondins as key regulators of synaptogenesis in the central nervous system, Matrix Biol., 31, 170-177, doi: 10.1016/j.matbio.2012.01.004.
  24. Eroglu, C., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Ozkan, E., Chakraborty, C., Mulinyawe, S. B., Annis, D. S., Huberman, A. D., Green, E. M., Lawler, J., Dolmetsch, R., Garcia, K. C., Smith, S. J., Luo, Z. D., Rosenthal, A., Mosher, D. F., and Barres, B. A. (2009) Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis, Cell, 139, 380-392, doi: 10.1016/j.cell.2009.09.025.
  25. Risher, W. C., and Eroglu, C. (2020) Astrocytes and synaptogenesis, in Synapse Development and Maturation, 2nd Edition, Acad. Press, pp. 55-75, doi: 10.1016/B978-0-12-823672-7.00003-X.
  26. 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., and Eroglu, C. (2018) Thrombospondin receptor α2δ-1 promotes synaptogenesis and spinogenesis via postsynaptic Rac1, J. Cell. Biol., 217, 3747-3765, doi: 10.1083/jcb.201802057.
  27. Xu, J., Xiao, N., and Xia, J. (2010) Thrombospondin 1 accelerates synaptogenesis in hippocampal neurons through neuroligin 1, Nat. Neurosci., 13, 22-24, doi: 10.1038/nn.2459.
  28. Stogsdill, J. A., Ramirez, J., Liu, D., Kim, Y. H., Baldwin, K. T., Enustun, E., Ejikeme, T., Ji, R. R., and Eroglu, C. (2017) Astrocytic neuroligins control astrocyte morphogenesis and synaptogenesis, Nature, 551, 192-197, doi: 10.1038/nature24638.
  29. Stogsdill, J. A., and Eroglu, C. (2017) The interplay between neurons and glia in synapse development and plasticity, Curr. Opin. Neurobiol., 42, 1-8, doi: 10.1016/j.conb.2016.09.016.
  30. Kucukdereli, H., Allen, N. J., Lee, A. T., Feng, A., Ozlu, M. I., Conatser, L. M., Chakraborty, C., Workman, G., Weaver, M., Sage, E. H., Barres, B. A., and Eroglu, C. (2011) Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC, Proc. Natl. Acad. Sci. USA, 108, E440-E449, doi: 10.1073/pnas.1104977108.
  31. Jones, E. V., Bernardinelli, Y., Tse, Y. C., Chierzi, S., Wong, T. P., and Murai, K. K. (2011) Astrocytes control glutamate receptor levels at developing synapses through SPARC-beta-integrin interactions, J. Neurosci., 31, 4154-4165, doi: 10.1523/JNEUROSCI.4757-10.2011.
  32. Singh, S. K., Stogsdill, J. A., Pulimood, N. S., Dingsdale, H., Kim, Y. H., Pilaz, L. J., Kim, I. H., Manhaes, A. C., Rodrigues, W. S. Jr., Pamukcu, A., Enustun, E., Ertuz, Z., Scheiffele, P., Soderling, S. H., Silver, D. L., Ji, R. R., Medina, A. E., and Eroglu, C. (2016) Astrocytes assemble thalamocortical synapses by bridging NRX1α and NL1 via Hevin, Cell, 164, 183-196, doi: 10.1016/j.cell.2015.11.034.
  33. Gan, K. J., and Südhof, T. C. (2020) SPARCL1 promotes excitatory but not inhibitory synapse formation and function independent of neurexins and neuroligins, J. Neurosci., 40, 8088-8102, doi: 10.1523/JNEUROSCI.0454-20.2020.
  34. Allen, N. J., and Eroglu, C. (2017) Cell biology of astrocyte-synapse interactions, Neuron, 96, 697-708, doi: 10.1016/j.neuron.2017.09.056.
  35. Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., and Barres, B. A. (2012) Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors, Nature, 486, 410-414, doi: 10.1038/nature11059.
  36. Farhy-Tselnicker, I., van Casteren, A. C. M., Lee, A., Chang, V. T., Aricescu, A. R., and Allen, N. J. (2017) Astrocyte-secreted glypican 4 regulates release of neuronal pentraxin 1 from axons to induce functional synapse formation, Neuron, 96, 428-445, doi: 10.1016/j.neuron.2017.09.053.
  37. Ko, J. S., Pramanik, G., Um, J. W., Shim, J. S., Lee, D., Kim, K. H., Chung, G. Y., Condomitti, G., Kim, H. M., Kim, H., de Wit, J., Park, K. S., Tabuchi, K., and Ko, J. (2015) PTPσ functions as a presynaptic receptor for the glypican-4/LRRTM4 complex and is essential for excitatory synaptic transmission, Proc. Natl. Acad. Sci. USA, 112, 1874-1879, doi: 10.1073/pnas.1410138112.
  38. Roppongi, R. T., Dhume, S. H., Padmanabhan, N., Silwal, P., Zahra, N., Karimi, B., Bomkamp, C., Patil, C. S., Champagne-Jorgensen, K., Twilley, R. E., Zhang, P., Jackson, M. F., and Siddiqui, T. J. (2020) LRRTMs organize synapses through differential engagement of neurexin and PTPσ, Neuron, 106, 108-125, doi: 10.1016/j.neuron.2020.05.003.
  39. Jean, Y. Y., Lercher, L. D., and Dreyfus, C. F. (2008) Glutamate elicits release of BDNF from basal forebrain astrocytes in a process dependent on metabotropic receptors and the PLC pathway, Neuron Glia Biol., 4, 35-42, doi: 10.1017/S1740925X09000052.
  40. De Pins, B., Cifuentes-Díaz, C., Farah, A. T., López-Molina, L., Montalban, E., Sancho-Balsells, A., López, A., Ginés, S., Delgado-García, J. M., Alberch, J., Gruart, A., Girault, J. A., and Giralt, A. (2019) Conditional BDNF delivery from astrocytes rescues memory deficits, spine density, and synaptic properties in the 5xFAD mouse model of Alzheimer's disease, J. Neurosci., 39, 2441-2458, doi: 10.1523/JNEUROSCI.2121-18.2019.
  41. Diniz, L. P., Tortelli, V., Garcia, M. N., Araújo, A. P., Melo, H. M., Silva, G. S., Felice, F. G., Alves-Leon, S. V., Souza, J. M., Romão, L. F., Castro, N. G., and Gomes, F. C. (2014) Astrocyte transforming growth factor beta 1 promotes inhibitory synapse formation via CaM kinase II signaling, Glia, 62, 1917-1931, doi: 10.1002/glia.22713.
  42. Diniz, L. P., Almeida, J. C., Tortelli, V., Vargas Lopes, C., Setti-Perdigão, P., Stipursky, J., Kahn, S. A., Romão, L. F., de Miranda, J., Alves-Leon, S. V., de Souza, J. M., Castro, N. G., Panizzutti, R., and Gomes, F. C. (2012) Astrocyte-induced synaptogenesis is mediated by transforming growth factor β signaling through modulation of D-serine levels in cerebral cortex neurons, J. Biol. Chem., 287, 41432-41445, doi: 10.1074/jbc.M112.380824.
  43. Diniz, L. P., Matias, I. C., Garcia, M. N., and Gomes, F. C. (2014) Astrocytic control of neural circuit formation: highlights on TGF-beta signaling, Neurochem. Int., 78, 18-27, doi: 10.1016/j.neuint.2014.07.008.
  44. Patel, M. R., and Weaver, A. M. (2021) Astrocyte-derived small extracellular vesicles promote synapse formation via fibulin-2-mediated TGF-β signaling, Cell. Rep., 34, 108829, doi: 10.1016/j.celrep.2021.108829.
  45. Blanco-Suarez, E., Liu, T. F., Kopelevich, A., and Allen, N. J. (2018) Astrocyte-secreted chordin-like 1 drives synapse maturation and limits plasticity by increasing synaptic GluA2 AMPA receptors, Neuron, 100, 1116-1132, doi: 10.1016/j.neuron.2018.09.043.
  46. Garrett, A. M., and Weiner, J. A. (2009) Control of CNS synapse development by γ-protocadherin-mediated astrocyte-neuron contact, J. Neurosci., 29, 11723-11731, doi: 10.1523/JNEUROSCI.2818-09.2009.
  47. Miralles, C. P., Taylor, M. J., Bear, J. Jr., Fekete, C. D., George, S., Li, Y., Bonhomme, B., Chiou, T. T., and De Blas, A. L. (2020) Expression of protocadherin-γC4 protein in the rat brain, J. Comp. Neurol., 528, 840-864, doi: 10.1002/cne.24783.
  48. Molumby, M. J., Anderson, R. M., Newbold, D. J., Koblesky, N. K., Garrett, A. M., Schreiner, D., Radley, J. J., and Weiner, J. A. (2017) γ-Protocadherins interact with neuroligin-1 and negatively regulate dendritic spine morphogenesis, Cell. Rep., 18, 2702-2714, doi: 10.1016/j.celrep.2017.02.060.
  49. Mauch, D. H., Nägler, K., Schumacher, S., Göritz, C., Müller, E. C., Otto, A., and Pfrieger, F. W. (2001) CNS synaptogenesis promoted by glia-derived cholesterol, Science, 294, 1354-1357, doi: 10.1126/science.294.5545.1354.
  50. Goritz, C., Mauch, D. H., and Pfrieger, F. W. (2005) Multiple mechanisms mediate cholesterol-induced synaptogenesis in a CNS neuron, Mol. Cell Neurosci., 29, 190-201, doi: 10.1016/j.mcn.2005.02.006.
  51. Goritz, C., Mauch, D. H., Nägler, K., and Pfrieger, F. W. (2002) Role of glia-derived cholesterol in synaptogenesis: new revelations in the synapse-glia affair, J. Physiol. Paris, 96, 257-263, doi: 10.1016/s0928-4257(02)00014-1.
  52. Pfrieger, F. W. (2003) Role of cholesterol in synapse formation and function, Biochim. Biophys. Acta, 1610, 271-280, doi: 10.1126/science.277.5332.1684.
  53. Wang, Y., Fu, A. K. Y., and Ip, N. Y. (2022) Instructive roles of astrocytes in hippocampal synaptic plasticity: neuronal activity-dependent regulatory mechanisms, FEBS J., 289, 2202-2218, doi: 10.1111/febs.15878.
  54. Van Deijk, A. F., Camargo, N., Timmerman, J., Heistek, T., Brouwers, J. F., Mogavero, F., Mansvelder, H. D., Smit, A. B., and Verheijen, M. H. (2017) Astrocyte lipid metabolism is critical for synapse development and function in vivo, Glia, 65, 670-682, doi: 10.1002/glia.23120.
  55. Ferris, H. A., Perry, R. J., Moreira, G. V., Shulman, G. I., Horton, J. D., and Kahn, C. R. (2017) Loss of astrocyte cholesterol synthesis disrupts neuronal function and alters whole-body metabolism, Proc. Natl. Acad. Sci. USA, 114, 1189-1194, doi: 10.1073/pnas.1620506114.
  56. Ebrahimi, M., Yamamoto, Y., Sharifi, K., Kida, H., Kagawa, Y., Yasumoto, Y., Islam, A., Miyazaki, H., Shimamoto, C., Maekawa, M., Mitsushima, D., Yoshikawa, T., and Owada, Y. (2016) Astrocyte-expressed FABP7 regulates dendritic morphology and excitatory synaptic function of cortical neurons, Glia, 64, 48-62, doi: 10.1002/glia.22902.
  57. Chiareli, R. A., Carvalho, G. A., Marques, B. L., Mota, L. S., Oliveira-Lima, O. C., Gomes, R. M., Birbrair, A., Gomez, R. S., Simão, F., Klempin, F., Leist, M., and Pinto, M. C. X. (2021) The role of astrocytes in the neurorepair process, Front. Cell. Dev. Biol., 9, 665795, doi: 10.3389/fcell.2021.665795.
  58. Fossati, G., Pozzi, D., Canzi, A., Mirabella, F., Valentino, S., Morini, R., Ghirardini, E., Filipello, F., Moretti, M., Gotti, C., Annis, D. S., Mosher, D. F., Garlanda, C., Bottazzi, B., Taraboletti, G., Mantovani, A., Matteoli, M., and Menna, E. (2019) Pentraxin 3 regulates synaptic function by inducing AMPA receptor clustering via ECM remodeling and β1-integrin, EMBO J., 38, e99529, doi: 10.15252/embj.201899529.
  59. Carmona, M. A., Murai, K. K., Wang, L., Roberts, A. J., and Pasquale, E. B. (2009) Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport, Proc. Natl. Acad. Sci. USA, 106, 12524-12529, doi: 10.1073/pnas.0903328106.
  60. Murai, K. K., and Pasquale, E. B. (2011) Eph receptors and ephrins in neuron-astrocyte communication at synapses, Glia, 59, 1567-1578, doi: 10.1002/glia.21226.
  61. Kania, A., and Klein, R. (2016) Mechanisms of ephrin-Eph signalling in development, physiology and disease, Nat. Rev. Mol. Cell Biol., 17, 240-256, doi: 10.1038/nrm.2015.16.
  62. Nguyen, A. Q., Koeppen, J., Woodruff, S., Mina, K., Figueroa, Z., and Ethell, I. M. (2020) Astrocytic ephrin-b1 controls synapse formation in the hippocampus during learning and memory, Front. Synaptic Neurosci., 12, 10, doi: 10.3389/fnsyn.2020.00010.
  63. Nguyen, A. Q., Sutley, S., Koeppen, J., Mina, K., Woodruff, S., Hanna, S., Vengala, A., Hickmott, P. W., Obenaus, A., and Ethell, I. M. (2020) Astrocytic ephrin-B1 controls excitatory-inhibitory balance in developing hippocampus, J. Neurosci., 40, 6854-6871, doi: 10.3389/fnsyn.2020.00010.
  64. Hung, C. Y., Hsu, T. I., Chuang, J. Y., Su, T. P., Chang, W. C., and Hung, J. J. (2020) Sp1 in astrocyte is important for neurite outgrowth and synaptogenesis, Mol. Neurobiol., 57, 261-277, doi: 10.1007/s12035-019-01694-7.
  65. Espírito-Santo, S., Coutinho, V. G., Dezonne, R. S., Stipursky, J., Dos Santos-Rodrigues, A., Batista, C., Paes-de-Carvalho, R., Fuss, B., and Gomes, F. C. A. (2021) Astrocytes as a target for Nogo-A and implications for synapse formation in vitro and in a model of acute demyelination, Glia, 69, 1429-1443, doi: 10.1002/glia.23971.
  66. Xie, Y., Kuan, A. T., Wang, W., Herbert, Z. T., Mosto, O., Olukoya, O., Adam, M., Vu, S., Kim, M., Tran, D., Gómez, N., Charpentier, C., Sorour, I., Lacey, T. E., Tolstorukov, M. Y., Sabatini, B. L., Lee, W. A., and Harwell, C. C. (2022) Astrocyte-neuron crosstalk through Hedgehog signaling mediates cortical synapse development, Cell. Rep., 38, 110416, doi: 10.1016/j.celrep.2022.110416.
  67. Zehnder, T., Petrelli, F., Romanos, J., De Oliveira Figueiredo, E. C., Lewis, T. L., Déglon, N., Polleux, F., Santello, M., and Bezzi, P. (2021) Mitochondrial biogenesis in developing astrocytes regulates astrocyte maturation and synapse formation, Cell. Rep., 35, 108952, doi: 10.1016/j.celrep.2021.108952.
  68. Risher, W. C., Patel, S., Kim, I. H., Uezu, A., Bhagat, S., Wilton, D. K., Pilaz, L. J., Singh Alvarado, J., Calhan, O. Y., Silver, D. L., Stevens, B., Calakos, N., Soderling, S. H., and Eroglu, C. (2014) Astrocytes refine cortical connectivity at dendritic spines, Elife, 3, e04047, doi: 10.7554/eLife.04047.
  69. Hennes, M., Lombaert, N., Wahis, J., Van den Haute, C., Holt, M. G., and Arckens, L. (2020) Astrocytes shape the plastic response of adult cortical neurons to vision loss, Glia, 68, 2102-2118, doi: 10.1002/glia.23830.
  70. Lawal, O., Ulloa Severino, F. P., and Eroglu, C. (2022) The role of astrocyte structural plasticity in regulating neural circuit function and behavior, Glia, 70, 1467-1483, doi: 10.1002/glia.24191.
  71. Lyon, K. A., and Allen, N. J. (2022) From synapses to circuits, astrocytes regulate behavior, Front. Neural Circuits, 15, 786293, doi: 10.3389/fncir.2021.786293.
  72. Chicurel, M. E., Terrian, D. M., and Potter, H. (1993) mRNA at the synapse: analysis of a synaptosomal preparation enriched in hippocampal dendritic spines, J. Neurosci., 13, 4054-4063, doi: 10.1523/JNEUROSCI.13-09-04054.1993.
  73. Baldwin, K. T., and Eroglu, C. (2018) Astrocytes "chordinate" synapse maturation and plasticity, Neuron, 100, 1010-1012, doi: 10.1016/j.neuron.2018.11.027.
  74. Bosworth, A. P., and Allen, N. J. (2017) The diverse actions of astrocytes during synaptic development, Curr. Opin. Neurobiol., 47, 38-43, doi: 10.1016/j.conb.2017.08.017.
  75. Liu, X., Ying, J., Wang, X., Zheng, Q., Zhao, T., Yoon, S., Yu, W., Yang, D., Fang, Y., and Hua, F. (2021) Astrocytes in neural circuits: key factors in synaptic regulation and potential targets for neurodevelopmental disorders, Front. Mol. Neurosci., 14, 729273, doi: 10.3389/fnmol.2021.729273.
  76. Sancho, L., Contreras, M., and Allen, N. J. (2021) Glia as sculptors of synaptic plasticity, Neurosci. Res., 167, 17-29, doi: 10.1016/j.neures.2020.11.005.
  77. Durkee, C., Kofuji, P., Navarrete, M., and Araque, A. (2021) Astrocyte and neuron cooperation in long-term depression, Trends Neurosci., 44, 837-848, doi: 10.1016/j.tins.2021.07.004.
  78. Ota, Y., Zanetti, A. T., and Hallock, R. M. (2013) The role of astrocytes in the regulation of synaptic plasticity and memory formation, Neural Plast., 2013, 185463, doi: 10.1155/2013/185463.
  79. Henneberger, C., Papouin, T., Oliet, S. H., and Rusakov, D. A. (2010) Long-term potentiation depends on release of D-serine from astrocytes, Nature, 463, 232-236, doi: 10.1038/nature08673.
  80. Adamsky, A., Kol, A., Kreisel, T., Doron, A., Ozeri-Engelhard, N., Melcer, T., Refaeli, R., Horn, H., Regev, L., Groysman, M., London, M., and Goshen, I. (2018) Astrocytic activation generates de novo neuronal potentiation and memory enhancement, Cell, 174, 59-71, doi: 10.1016/j.cell.2018.05.002.
  81. Masuoka, T., Ikeda, R., and Konishi, S. (2019) Persistent activation of histamine H1 receptors in the hippocampal CA1 region enhances NMDA receptor-mediated synaptic excitation and long-term potentiation in astrocyte- and D-serine-dependent manner, Neuropharmacology, 151, 64-73, doi: 10.1016/j.neuropharm.2019.03.036.
  82. Cavaccini, A., Durkee, C., Kofuji, P., Tonini, R., and Araque, A. (2020) Astrocyte signaling gates long-term depression at corticostriatal synapses of the direct pathway, J. Neurosci., 40, 5757-5768, doi: 10.1523/JNEUROSCI.2369-19.2020.
  83. 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., and Rodríguez-Moreno, A. (2020) Astrocyte-mediated switch in spike timing-dependent plasticity during hippocampal development, Nat. Commun., 11, 4388, doi: 10.1038/s41467-020-18024-4.
  84. Lee, C. J., Mannaioni, G., Yuan, H., Woo, D. H., Gingrich, M. B., and Traynelis, S. F. (2007) Astrocytic control of synaptic NMDA receptors, J. Physiol., 581, 1057-1081, doi: 10.1113/jphysiol.2007.130377.
  85. Park, H., Han, K. S., Seo, J., Lee, J., Dravid, S. M., Woo, J., Chun, H., Cho, S., Bae, J. Y., An, H., Koh, W., Yoon, B. E., Berlinguer-Palmini, R., Mannaioni, G., Traynelis, S. F., Bae, Y. C., Choi, S. Y., and Lee, C. J. (2015) Channel-mediated astrocytic glutamate modulates hippocampal synaptic plasticity by activating postsynaptic NMDA receptors, Mol. Brain, 8, 7, doi: 10.1186/s13041-015-0097-y.
  86. 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., and Esteban, J. A. (2019) Astrocytic p38α MAPK drives NMDA receptor-dependent long-term depression and modulates long-term memory, Nat. Commun., 10, 2968, doi: 10.1038/s41467-019-10830.
  87. Boué-Grabot, E., and Pankratov, Y. (2017) Modulation of central synapses by astrocyte-released ATP and postsynaptic P2X receptors, Neural Plast., 2017, 9454275, doi: 10.1155/2017/9454275.
  88. Crosby, K. M., Murphy-Royal, C., Wilson, S. A., Gordon, G. R., Bains, J. S., and Pittman, Q. J. (2018) Cholecystokinin switches the plasticity of GABA synapses in the dorsomedial hypothalamus via astrocytic ATP release, J. Neurosci., 38, 8515-8525, doi: 10.1523/JNEUROSCI.0569-18.2018.
  89. Covelo, A., Eraso-Pichot, A., Fernández-Moncada, I., Serrat, R., and Marsicano, G. (2021) CB1R-dependent regulation of astrocyte physiology and astrocyte-neuron interactions, Neuropharmacology, 195, 108678, doi: 10.1016/j.neuropharm.2021.108678.
  90. Martin-Fernandez, M., Jamison, S., Robin, L. M., Zhao, Z., Martin, E. D., Aguilar, J., Benneyworth, M. A., Marsicano, G., and Araque, A. (2017) Synapse-specific astrocyte gating of amygdala-related behavior, Nat. Neurosci., 20, 1540-1548, doi: 10.1038/nn.4649.
  91. 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., and Marsicano, G. (2018) Astroglial CB1 receptors determine synaptic D-serine availability to enable recognition memory, Neuron, 98, 935-944, doi: 10.1016/j.neuron.2018.04.034.
  92. Durieux, L. J. A., Gilissen, S. R. J., and Arckens, L. (2022) Endocannabinoids and cortical plasticity: CB1R as a possible regulator of the excitation/inhibition balance in health and disease, Eur. J. Neurosci., 55, 971-988, doi: 10.1111/ejn.15110.
  93. Balschun, D., Wetzel, W., Del Rey, A., Pitossi, F., Schneider, H., Zuschratter, W., and Besedovsky, H. O. (2004) Interleukin-6: a cytokine to forget, FASEB J., 18, 1788-1790, doi: 10.1096/fj.04-1625fje.
  94. Quintana, A., Erta, M., Ferrer, B., Comes, G., Giralt, M., and Hidalgo, J. (2013) Astrocyte-specific deficiency of interleukin-6 and its receptor reveal specific roles in survival, body weight and behavior, Brain Behav. Immun., 27, 162-173, doi: 10.1016/j.bbi.2012.10.011.
  95. Roberts, A. J., Khom, S., Bajo, M., Vlkolinsky, R., Polis, I., Cates-Gatto, C., Roberto, M., and Gruol, D. L. (2019) Increased IL-6 expression in astrocytes is associated with emotionality, alterations in central amygdala GABAergic transmission, and excitability during alcohol withdrawal, Brain Behav. Immun., 82, 188-202, doi: 10.1016/j.bbi.2019.08.185.
  96. Alberini, C. M., Cruz, E., Descalzi, G., Bessières, B., and Gao, V. (2018) Astrocyte glycogen and lactate: new insights into learning and memory mechanisms, Glia, 66, 1244-1262, doi: 10.1002/glia.23250.
  97. Suzuki, A., Stern, S. A., Bozdagi, O., Huntley, G. W., Walker, R. H., Magistretti, P. J., and Alberini, C. M. (2011) Astrocyte-neuron lactate transport is required for long-term memory formation, Cell, 144, 810-823, doi: 10.1016/j.cell.2011.02.018.
  98. Descalzi, G., Gao, V., Steinman, M. Q., Suzuki, A., and Alberini, C. M. (2019) Lactate from astrocytes fuels learning-induced mRNA translation in excitatory and inhibitory neurons, Commun. Biol., 2, 247, doi: 10.1038/s42003-019-0495-2.
  99. Duran, J., Brewer, M. K., Hervera, A., Gruart, A., Del Rio, J. A., Delgado-García, J. M., and Guinovart, J. J. (2020) Lack of astrocytic glycogen alters synaptic plasticity but not seizure susceptibility, Mol. Neurobiol., 57, 4657-4666, doi: 10.1007/s12035-020-02055-5.
  100. Vezzoli, E., Calì, C., De Roo, M., Ponzoni, L., Sogne, E., Gagnon, N., Francolini, M., Braida, D., Sala, M., Muller, D., Falqui, A., and Magistretti, P. J. (2020) Ultrastructural evidence for a role of astrocytes and glycogen-derived lactate in learning-dependent synaptic stabilization, Cereb. Cortex, 30, 2114-2127, doi: 10.1093/cercor/bhz226.
  101. 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., and Soderling, S. H. (2020) Chemico-genetic discovery of astrocytic control of inhibition in vivo, Nature, 588, 296-302, doi: 10.1038/s41586-020-2926-0.

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