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Neural Plasticity
Volume 2017, Article ID 9454275, 11 pages
https://doi.org/10.1155/2017/9454275
Review Article

Modulation of Central Synapses by Astrocyte-Released ATP and Postsynaptic P2X Receptors

1Institut des Maladies Neurodégénératives, University Bordeaux, UMR 5293, 33000 Bordeaux, France
2Institut des Maladies Neurodégénératives, CNRS, UMR 5293, 33000 Bordeaux, France
3School of Life Sciences, University of Warwick, Coventry, UK
4School of Life Sciences, Immanuel Kant Baltic Federal University, Kaliningrad, Russia

Correspondence should be addressed to Eric Boué-Grabot; rf.xuaedrob-u@tobarg-euob.cire

Received 24 March 2017; Accepted 10 July 2017; Published 6 August 2017

Academic Editor: Antonio Pinto-Duarte

Copyright © 2017 Eric Boué-Grabot and Yuriy Pankratov. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Burnstock, “Physiology and pathophysiology of purinergic neurotransmission,” Physiological Reviews, vol. 87, no. 2, pp. 659–797, 2007. View at Google Scholar
  2. A. M. Butt, “ATP: a ubiquitous gliotransmitter integrating neuron-glial networks,” Seminars in Cell & Developmental Biology, vol. 22, no. 2, pp. 205–213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. R. D. Fields and G. Burnstock, “Purinergic signalling in neuron-glia interactions,” Nature Reviews Neuroscience, vol. 7, no. 6, pp. 423–436, 2006. View at Google Scholar
  4. R. D. Fields and B. Stevens, “ATP: an extracellular signaling molecule between neurons and glia,” Trends in Neurosciences, vol. 23, no. 12, pp. 625–633, 2000. View at Google Scholar
  5. U. Lalo, A. Verkhratsky, and Y. Pankratov, “Ionotropic ATP receptors in neuronal-glial communication,” Seminars in Cell & Developmental Biology, vol. 22, no. 2, pp. 220–228, 2011. View at Google Scholar
  6. K. Harada, T. Kamiya, and T. Tsuboi, “Gliotransmitter release from astrocytes: functional, developmental, and pathological implications in the brain,” Frontiers in Neuroscience, vol. 9, p. 499, 2016. View at Google Scholar
  7. A. M. Sebastiao and J. A. Ribeiro, “Adenosine receptors and the central nervous system,” Handbook of Experimental Pharmacology, vol. 193, pp. 471–534, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Popoli and R. Pepponi, “Potential therapeutic relevance of adenosine A2B and A2A receptors in the central nervous system,” CNS & Neurological Disorders Drug Targets, vol. 11, no. 6, pp. 664–674, 2012. View at Google Scholar
  9. S. Paul, P. H. Elsinga, K. Ishiwata, R. A. Dierckx, and A. Waarde, “Adenosine A(1) receptors in the central nervous system: their functions in health and disease, and possible elucidation by PET imaging,” Current Medicinal Chemistry, vol. 18, no. 31, pp. 4820–4835, 2011. View at Google Scholar
  10. R. J. Rodrigues, A. R. Tome, and R. A. Cunha, “ATP as a multi-target danger signal in the brain,” Frontiers in Neuroscience, vol. 9, p. 148, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. M. P. Abbracchio, G. Burnstock, A. Verkhratsky, and H. Zimmermann, “Purinergic signalling in the nervous system: an overview,” Trends in Neurosciences, vol. 32, no. 1, pp. 19–29, 2009. View at Google Scholar
  12. B. S. Khakh and R. A. North, “Neuromodulation by extracellular ATP and P2X receptors in the CNS,” Neuron, vol. 76, no. 1, pp. 51–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. Pankratov and U. Lalo, “Calcium permeability of ligand-gated Ca2+ channels,” European Journal of Pharmacology, vol. 739, pp. 60–73, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. G. A. Weisman, L. T. Woods, L. Erb, and C. I. Seye, “P2Y receptors in the mammalian nervous system: pharmacology, ligands and therapeutic potential,” CNS & Neurological Disorders Drug Targets, vol. 11, no. 6, pp. 722–738, 2012. View at Google Scholar
  15. R. J. Rodrigues, T. Almeida, P. J. Richardson, C. R. Oliveira, and R. A. Cunha, “Dual presynaptic control by ATP of glutamate release via facilitatory P2X1, P2X2/3, and P2X3 and inhibitory P2Y1, P2Y2, and/or P2Y4 receptors in the rat hippocampus,” The Journal of Neuroscience, vol. 25, no. 27, pp. 6286–6295, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. M. E. Rubio and F. Soto, “Distinct localization of P2X receptors at excitatory postsynaptic specializations,” The Journal of Neuroscience, vol. 21, no. 2, pp. 641–653, 2001. View at Google Scholar
  17. V. Vavra, A. Bhattacharya, and H. Zemkova, “Facilitation of glutamate and GABA release by P2X receptor activation in supraoptic neurons from freshly isolated rat brain slices,” Neuroscience, vol. 188, pp. 1–12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. B. S. Khakh and R. A. North, “P2X receptors as cell-surface ATP sensors in health and disease,” Nature, vol. 442, no. 7102, pp. 527–532, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. A. V. Gourine, V. Kasymov, N. Marina et al., “Astrocytes control breathing through pH-dependent release of ATP,” Science, vol. 329, no. 5991, pp. 571–575, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. M. M. Halassa, T. Fellin, and P. G. Haydon, “The tripartite synapse: roles for gliotransmission in health and disease,” Trends in Molecular Medicine, vol. 13, no. 2, pp. 54–63, 2007. View at Google Scholar
  21. M. M. Halassa, C. Florian, T. Fellin et al., “Astrocytic modulation of sleep homeostasis and cognitive consequences of sleep loss,” Neuron, vol. 61, no. 2, pp. 213–219, 2009. View at Google Scholar
  22. E. Beamer, F. Goloncser, G. Horvath et al., “Purinergic mechanisms in neuroinflammation: an update from molecules to behavior,” Neuropharmacology, vol. 104, pp. 94–104, 2016. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Beggs, T. Trang, and M. W. Salter, “P2X4R+ microglia drive neuropathic pain,” Nature Neuroscience, vol. 15, no. 8, pp. 1068–1073, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. J. George, R. A. Cunha, C. Mulle, and T. Amedee, “Microglia-derived purines modulate mossy fibre synaptic transmission and plasticity through P2X4 and A1 receptors,” The European Journal of Neuroscience, vol. 43, no. 10, pp. 1366–1378, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Araque, V. Parpura, R. P. Sanzgiri, and P. G. Haydon, “Tripartite synapses: glia, the unacknowledged partner,” Trends in Neurosciences, vol. 22, no. 5, pp. 208–215, 1999. View at Google Scholar
  26. A. Araque, G. Carmignoto, P. G. Haydon, S. H. Oliet, R. Robitaille, and A. Volterra, “Gliotransmitters travel in time and space,” Neuron, vol. 81, no. 4, pp. 728–739, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. N. B. Hamilton and D. Attwell, “Do astrocytes really exocytose neurotransmitters?” Nature Reviews Neuroscience, vol. 11, no. 4, pp. 227–238, 2010. View at Google Scholar
  28. U. Lalo, O. Palygin, S. Rasooli-Nejad, J. Andrew, P. G. Haydon, and Y. Pankratov, “Exocytosis of ATP from astrocytes modulates phasic and tonic inhibition in the neocortex,” PLoS Biology, vol. 12, no. 1, article e1001747, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. Z. Zhang, G. Chen, W. Zhou et al., “Regulated ATP release from astrocytes through lysosome exocytosis,” Nature Cell Biology, vol. 9, no. 8, pp. 945–953, 2007. View at Publisher · View at Google Scholar
  30. G. R. Gordon, D. V. Baimoukhametova, S. A. Hewitt, W. R. Rajapaksha, T. E. Fisher, and J. S. Bains, “Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy,” Nature Neuroscience, vol. 8, no. 8, pp. 1078–1086, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. G. R. Gordon, K. J. Iremonger, S. Kantevari, G. C. Ellis-Davies, B. A. MacVicar, and J. S. Bains, “Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses,” Neuron, vol. 64, no. 3, pp. 391–403, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. U. Lalo, O. Palygin, A. Verkhratsky, S. G. Grant, and Y. Pankratov, “ATP from synaptic terminals and astrocytes regulates NMDA receptors and synaptic plasticity through PSD-95 multi-protein complex,” Scientific Reports, vol. 6, article 33609, 2016. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Rasooli-Nejad, O. Palygin, U. Lalo, and Y. Pankratov, “Cannabinoid receptors contribute to astroglial Ca(2)(+)-signalling and control of synaptic plasticity in the neocortex,” Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, vol. 369, no. 1654, article 20140077, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. S. A. Sloan and B. A. Barres, “Looks can be deceiving: reconsidering the evidence for gliotransmission,” Neuron, vol. 84, no. 6, pp. 1112–1115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Sultan, L. Li, J. Moss et al., “Synaptic integration of adult-born hippocampal neurons is locally controlled by astrocytes,” Neuron, vol. 88, no. 5, pp. 957–972, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Papouin, J. M. Dunphy, M. Tolman, K. T. Dineley, and P. G. Haydon, “Septal cholinergic neuromodulation tunes the astrocyte-dependent gating of hippocampal NMDA receptors to wakefulness,” Neuron, vol. 94, no. 4, pp. 840–854, 2017, e7. View at Publisher · View at Google Scholar
  37. J. M. Garre, M. A. Retamal, P. Cassina et al., “FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 52, pp. 22659–22664, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Volonte, S. Amadio, F. Cavaliere, N. D'Ambrosi, F. Vacca, and G. Bernardi, “Extracellular ATP and neurodegeneration,” Current Drug Targets CNS and Neurological Disorders, vol. 2, no. 6, pp. 403–412, 2003. View at Google Scholar
  39. U. Lalo, S. Rasooli-Nejad, and Y. Pankratov, “Exocytosis of gliotransmitters from cortical astrocytes: implications for synaptic plasticity and aging,” Biochemical Society Transactions, vol. 42, no. 5, pp. 1275–1281, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. J. T. Pougnet, E. Toulme, A. Martinez, D. Choquet, E. Hosy, and E. Boue-Grabot, “ATP P2X receptors downregulate AMPA receptor trafficking and postsynaptic efficacy in hippocampal neurons,” Neuron, vol. 83, no. 2, pp. 417–430, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. F. A. Edwards, A. J. Gibb, and D. Colquhoun, “ATP receptor-mediated synaptic currents in the central nervous system,” Nature, vol. 359, no. 6391, pp. 144–147, 1992. View at Google Scholar
  42. F. A. Edwards, S. J. Robertson, and A. J. Gibb, “Properties of ATP receptor-mediated synaptic transmission in the rat medial habenula,” Neuropharmacology, vol. 36, no. 9, pp. 1253–1268, 1997. View at Google Scholar
  43. Y. H. Jo and R. Schlichter, “Synaptic corelease of ATP and GABA in cultured spinal neurons,” Nature Neuroscience, vol. 2, no. 3, pp. 241–245, 1999. View at Google Scholar
  44. Y. Pankratov, U. Lalo, O. Krishtal, and A. Verkhratsky, “Ionotropic P2X purinoreceptors mediate synaptic transmission in rat pyramidal neurones of layer II/III of somato-sensory cortex,” The Journal of Physiology, vol. 542, Part 2, pp. 529–536, 2002. View at Google Scholar
  45. Y. Pankratov, U. Lalo, A. Verkhratsky, and R. A. North, “Quantal release of ATP in mouse cortex,” The Journal of General Physiology, vol. 129, no. 3, pp. 257–265, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. V. Pankratov, U. V. Lalo, and O. A. Krishtal, “Role for P2X receptors in long-term potentiation,” The Journal of Neuroscience, vol. 22, no. 19, pp. 8363–8369, 2002. View at Google Scholar
  47. Y. H. Jo and L. W. Role, “Coordinate release of ATP and GABA at in vitro synapses of lateral hypothalamic neurons,” The Journal of Neuroscience, vol. 22, no. 12, pp. 4794–4804, 2002. View at Google Scholar
  48. E. Boue-Grabot, “Interactions between ligand-gated ion channels: a new regulation mechanism for fast synaptic signaling?” Tech. Rep., Amino Acid Receptor Research Nova Science Publishers, 2008. View at Google Scholar
  49. J. T. Pougnet, B. Compans, A. Martinez, D. Choquet, E. Hosy, and E. Boue-Grabot, “P2X-mediated AMPA receptor internalization and synaptic depression is controlled by two CaMKII phosphorylation sites on GluA1 in hippocampal neurons,” Scientific Reports, vol. 6, article 31836, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Gomez-Villafuertes, J. Gualix, and M. T. Miras-Portugal, “Single GABAergic synaptic terminals from rat midbrain exhibit functional P2X and dinucleotide receptors, able to induce GABA secretion,” Journal of Neurochemistry, vol. 77, no. 1, pp. 84–93, 2001. View at Google Scholar
  51. J. G. Gu and A. B. MacDermott, “Activation of ATP P2X receptors elicits glutamate release from sensory neuron synapses,” Nature, vol. 389, no. 6652, pp. 749–753, 1997. View at Publisher · View at Google Scholar · View at Scopus
  52. R. A. Cunha and J. A. Ribeiro, “ATP as a presynaptic modulator,” Life Sciences, vol. 68, no. 2, pp. 119–137, 2000. View at Google Scholar
  53. M. Mori, C. Heuss, B. H. Gahwiler, and U. Gerber, “Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures,” The Journal of Physiology, vol. 535, Part 1, pp. 115–123, 2001. View at Google Scholar
  54. G. H. Hansen, E. Hosli, B. Belhage, A. Schousboe, and L. Hosli, “Light and electron microscopic localization of GABAA-receptors on cultured cerebellar granule cells and astrocytes using immunohistochemical techniques,” Neurochemical Research, vol. 16, no. 3, pp. 341–346, 1991. View at Google Scholar
  55. A. Baude, Z. Nusser, E. Molnar, R. A. McIlhinney, and P. Somogyi, “High-resolution immunogold localization of AMPA type glutamate receptor subunits at synaptic and non-synaptic sites in rat hippocampus,” Neuroscience, vol. 69, no. 4, pp. 1031–1055, 1995. View at Google Scholar
  56. A. Triller and D. Choquet, “Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!,” Trends in Neurosciences, vol. 28, no. 3, pp. 133–139, 2005. View at Google Scholar
  57. E. Toulme and B. S. Khakh, “Imaging P2X4 receptor lateral mobility in microglia: regulation by calcium and p38 MAPK,” The Journal of Biological Chemistry, vol. 287, no. 18, pp. 14734–14748, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Richler, E. Shigetomi, and B. S. Khakh, “Neuronal P2X2 receptors are mobile ATP sensors that explore the plasma membrane when activated,” The Journal of Neuroscience, vol. 31, no. 46, pp. 16716–16730, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. L. K. Bobanovic, S. J. Royle, and R. D. Murrell-Lagnado, “P2X receptor trafficking in neurons is subunit specific,” The Journal of Neuroscience, vol. 22, no. 12, pp. 4814–4824, 2002. View at Google Scholar
  60. Y. H. Jo, E. Donier, A. Martinez, M. Garret, E. Toulme, and E. Boue-Grabot, “Cross-talk between P2X4 and gamma-aminobutyric acid, type A receptors determines synaptic efficacy at a central synapse,” The Journal of Biological Chemistry, vol. 286, no. 22, pp. 19993–20004, 2011. View at Google Scholar
  61. S. J. Royle, L. K. Bobanovic, and R. D. Murrell-Lagnado, “Identification of a non-canonical tyrosine-based endocytic motif in an ionotropic receptor,” The Journal of Biological Chemistry, vol. 277, no. 38, pp. 35378–35385, 2002. View at Google Scholar
  62. S. J. Royle, O. S. Qureshi, L. K. Bobanovic, P. R. Evans, D. J. Owen, and R. D. Murrell-Lagnado, “Non-canonical YXXGPhi endocytic motifs: recognition by AP2 and preferential utilization in P2X4 receptors,” Journal of Cell Science, vol. 118, Part 14, pp. 3073–3080, 2005. View at Google Scholar
  63. E. Toulme, A. Garcia, D. Samways, T. M. Egan, M. J. Carson, and B. S. Khakh, “P2X4 receptors in activated C8-B4 cells of cerebellar microglial origin,” The Journal of General Physiology, vol. 135, no. 4, pp. 333–353, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. L. E. Robinson and R. D. Murrell-Lagnado, “The trafficking and targeting of P2X receptors,” Frontiers in Cellular Neuroscience, vol. 7, p. 233, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. R. Varma, Y. Chai, J. Troncoso et al., “Amyloid-beta induces a caspase-mediated cleavage of P2X4 to promote purinotoxicity,” Neuromolecular Medicine, vol. 11, no. 2, pp. 63–75, 2009. View at Google Scholar
  66. A. Casanovas, S. Hernandez, O. Tarabal, J. Rossello, and J. E. Esquerda, “Strong P2X4 purinergic receptor-like immunoreactivity is selectively associated with degenerating neurons in transgenic rodent models of amyotrophic lateral sclerosis,” The Journal of Comparative Neurology, vol. 506, no. 1, pp. 75–92, 2008. View at Google Scholar
  67. S. Hernandez, A. Casanovas, L. Piedrafita, O. Tarabal, and J. E. Esquerda, “Neurotoxic species of misfolded SOD1G93A recognized by antibodies against the P2X4 subunit of the ATP receptor accumulate in damaged neurons of transgenic animal models of amyotrophic lateral sclerosis,” Journal of Neuropathology and Experimental Neurology, vol. 69, no. 2, pp. 176–187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  68. H. W. Kessels and R. Malinow, “Synaptic AMPA receptor plasticity and behavior,” Neuron, vol. 61, no. 3, pp. 340–350, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Malinow and R. C. Malenka, “AMPA receptor trafficking and synaptic plasticity,” Annual Review of Neuroscience, vol. 25, pp. 103–126, 2002. View at Google Scholar
  70. M. Heine, L. Groc, R. Frischknecht et al., “Surface mobility of postsynaptic AMPARs tunes synaptic transmission,” Science, vol. 320, no. 5873, pp. 201–205, 2008. View at Google Scholar
  71. S. F. Traynelis, L. P. Wollmuth, C. J. McBain et al., “Glutamate receptor ion channels: structure, regulation, and function,” Pharmacological Reviews, vol. 62, no. 3, pp. 405–496, 2010. View at Publisher · View at Google Scholar · View at Scopus
  72. R. A. Nicoll, S. Tomita, and D. S. Bredt, “Auxiliary subunits assist AMPA-type glutamate receptors,” Science, vol. 311, no. 5765, pp. 1253–1256, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. V. Anggono and R. L. Huganir, “Regulation of AMPA receptor trafficking and synaptic plasticity,” Current Opinion in Neurobiology, vol. 22, no. 3, pp. 461–469, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. V. Compan, L. Ulmann, O. Stelmashenko, J. Chemin, S. Chaumont, and F. Rassendren, “P2X2 and P2X5 subunits define a new heteromeric receptor with P2X7-like properties,” The Journal of Neuroscience, vol. 32, no. 12, pp. 4284–4296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  75. M. Paukert, A. Agarwal, J. Cha, V. A. Doze, J. U. Kang, and D. E. Bergles, “Norepinephrine controls astroglial responsiveness to local circuit activity,” Neuron, vol. 82, no. 6, pp. 1263–1270, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Ding, J. O'Donnell, A. S. Thrane et al., “α1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice,” Cell Calcium, vol. 54, no. 6, pp. 387–394, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Pankratov, U. Lalo, O. A. Krishtal, and A. Verkhratsky, “P2X receptors and synaptic plasticity,” Neuroscience, vol. 158, no. 1, pp. 137–148, 2009. View at Google Scholar
  78. J. A. Sim, S. Chaumont, J. Jo et al., “Altered hippocampal synaptic potentiation in P2X4 knock-out mice,” The Journal of Neuroscience, vol. 26, no. 35, pp. 9006–9009, 2006. View at Google Scholar
  79. S. D. Silberberg, M. Li, and K. J. Swartz, “Ivermectin interaction with transmembrane helices reveals widespread rearrangements during opening of P2X receptor channels,” Neuron, vol. 54, no. 2, pp. 263–274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. E. Toulme, F. Soto, M. Garret, and E. Boue-Grabot, “Functional properties of internalization-deficient P2X4 receptors reveal a novel mechanism of ligand-gated channel facilitation by ivermectin,” Molecular Pharmacology, vol. 69, no. 2, pp. 576–587, 2006. View at Google Scholar
  81. A. W. Baxter, S. J. Choi, J. A. Sim, and R. A. North, “Role of P2X4 receptors in synaptic strengthening in mouse CA1 hippocampal neurons,” The European Journal of Neuroscience, vol. 34, no. 2, pp. 213–220, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Migaud, P. Charlesworth, M. Dempster et al., “Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein,” Nature, vol. 396, no. 6710, pp. 433–439, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. J. Nithianantharajah, N. H. Komiyama, A. McKechanie et al., “Synaptic scaffold evolution generated components of vertebrate cognitive complexity,” Nature Neuroscience, vol. 16, no. 1, pp. 16–24, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. L. Atkinson, T. F. Batten, and J. Deuchars, “P2X(2) receptor immunoreactivity in the dorsal vagal complex and area postrema of the rat,” Neuroscience, vol. 99, no. 4, pp. 683–696, 2000. View at Google Scholar
  85. M. J. Neal, J. R. Cunningham, and Z. Dent, “Modulation of extracellular GABA levels in the retina by activation of glial P2X-purinoceptors,” British Journal of Pharmacology, vol. 124, no. 2, pp. 317–322, 1998. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. H. Jo and E. Boue-Grabot, “Interplay between ionotropic receptors modulates inhibitory synaptic strength,” Communicative & Integrative Biology, vol. 4, no. 6, pp. 706–709, 2011. View at Google Scholar
  87. B. S. Khakh, J. A. Fisher, R. Nashmi, D. N. Bowser, and H. A. Lester, “An angstrom scale interaction between plasma membrane ATP-gated P2X2 and alpha4beta2 nicotinic channels measured with fluorescence resonance energy transfer and total internal reflection fluorescence microscopy,” The Journal of Neuroscience, vol. 25, no. 29, pp. 6911–6920, 2005. View at Google Scholar
  88. B. S. Khakh, X. Zhou, J. Sydes, J. J. Galligan, and H. A. Lester, “State-dependent cross-inhibition between transmitter-gated cation channels,” Nature, vol. 406, no. 6794, pp. 405–410, 2000. View at Google Scholar
  89. E. Boue-Grabot, C. Barajas-Lopez, Y. Chakfe et al., “Intracellular cross talk and physical interaction between two classes of neurotransmitter-gated channels,” The Journal of Neuroscience, vol. 23, no. 4, pp. 1246–1253, 2003. View at Google Scholar
  90. E. Boue-Grabot, M. B. Emerit, E. Toulme, P. Seguela, and M. Garret, “Cross-talk and co-trafficking between rho1/GABA receptors and ATP-gated channels,” The Journal of Biological Chemistry, vol. 279, no. 8, pp. 6967–6975, 2004. View at Google Scholar
  91. E. Boue-Grabot, E. Toulme, M. B. Emerit, and M. Garret, “Subunit-specific coupling between gamma-aminobutyric acid type A and P2X2 receptor channels,” The Journal of Biological Chemistry, vol. 279, no. 50, pp. 52517–52525, 2004. View at Publisher · View at Google Scholar · View at Scopus
  92. E. Toulme, D. Blais, C. Leger et al., “An intracellular motif of P2X(3) receptors is required for functional cross-talk with GABA(A) receptors in nociceptive DRG neurons,” Journal of Neurochemistry, vol. 102, no. 4, pp. 1357–1368, 2007. View at Google Scholar
  93. M. B. Emerit, C. Baranowski, J. Diaz et al., “A new mechanism of receptor targeting by interaction between two classes of ligand-gated ion channels,” The Journal of Neuroscience, vol. 36, no. 5, pp. 1456–1470, 2016. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Pankratov and U. Lalo, “Role for astroglial alpha1-adrenoreceptors in gliotransmission and control of synaptic plasticity in the neocortex,” Frontiers in Cellular Neuroscience, vol. 9, p. 230, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Viana da Silva, M. G. Haberl, P. Zhang et al., “Early synaptic deficits in the APP/PS1 mouse model of Alzheimer’s disease involve neuronal adenosine A2A receptors,” Nature Communications, vol. 7, article 11915, 2016. View at Publisher · View at Google Scholar · View at Scopus
  96. S. R. Hulme, O. D. Jones, C. R. Raymond, P. Sah, and W. C. Abraham, “Mechanisms of heterosynaptic metaplasticity,” Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, vol. 369, no. 1633, article 20130148, 2014. View at Publisher · View at Google Scholar · View at Scopus
  97. B. Strooper and E. Karran, “The cellular phase of Alzheimer’s disease,” Cell, vol. 164, no. 4, pp. 603–615, 2016. View at Publisher · View at Google Scholar · View at Scopus
  98. J. J. Rodriguez-Arellano, V. Parpura, R. Zorec, and A. Verkhratsky, “Astrocytes in physiological aging and Alzheimer’s disease,” Neuroscience, vol. 323, pp. 170–182, 2016. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Keck, T. Toyoizumi, L. Chen et al., “Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions,” Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, vol. 372, no. 1715, 2017. View at Publisher · View at Google Scholar
  100. T. Takeuchi, A. J. Duszkiewicz, and R. G. Morris, “The synaptic plasticity and memory hypothesis: encoding, storage and persistence,” Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, vol. 369, no. 1633, article 20130288, 2014. View at Publisher · View at Google Scholar · View at Scopus
  101. B. S. Khakh and K. D. McCarthy, “Astrocyte calcium signaling: from observations to functions and the challenges therein,” Cold Spring Harbor Perspectives in Biology, vol. 7, no. 4, article a020404, 2015. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Panatier, J. Vallee, M. Haber, K. K. Murai, J. C. Lacaille, and R. Robitaille, “Astrocytes are endogenous regulators of basal transmission at central synapses,” Cell, vol. 146, no. 5, pp. 785–798, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. R. Martin, R. Bajo-Graneras, R. Moratalla, G. Perea, and A. Araque, “Circuit-specific signaling in astrocyte-neuron networks in basal ganglia pathways,” Science, vol. 349, no. 6249, pp. 730–734, 2015. View at Publisher · View at Google Scholar · View at Scopus
  104. M. P. Kummer, T. Hammerschmidt, A. Martinez et al., “Ear2 deletion causes early memory and learning deficits in APP/PS1 mice,” The Journal of Neuroscience, vol. 34, no. 26, pp. 8845–8854, 2014. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Nithianantharajah and A. J. Hannan, “The neurobiology of brain and cognitive reserve: mental and physical activity as modulators of brain disorders,” Progress in Neurobiology, vol. 89, no. 4, pp. 369–382, 2009. View at Google Scholar