Long-term potentiation depends on release of d-serine from astrocytes (original) (raw)

References

  1. Bliss, T. V. P. & Collingridge, G. L. A synaptic model of memory—long-term potentiation in the hippocampus. Nature 361, 31–39 (1993)
    Article ADS CAS Google Scholar
  2. Schell, M. J., Molliver, M. E. & Snyder, S. H. d-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc. Natl Acad. Sci. USA 92, 3948–3952 (1995)
    Article ADS CAS Google Scholar
  3. Mothet, J. P. et al. d-Serine is an endogenous ligand for the glycine site of the _N_-methyl-d-aspartate receptor. Proc. Natl Acad. Sci. USA 97, 4926–4931 (2000)
    Article ADS CAS Google Scholar
  4. Panatier, A. et al. Glia-derived d-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775–784 (2006)
    Article CAS Google Scholar
  5. Yang, Y. et al. Contribution of astrocytes to hippocampal long-term potentiation through release of d-serine. Proc. Natl Acad. Sci. USA 100, 15194–15199 (2003)
    Article ADS CAS Google Scholar
  6. Bezzi, P. et al. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391, 281–285 (1998)
    Article ADS CAS Google Scholar
  7. Fellin, T. et al. Neuronal synchrony mediated by astrocytic glutamate through activation of extrasynaptic NMDA receptors. Neuron 43, 729–743 (2004)
    Article CAS Google Scholar
  8. Perea, G. & Araque, A. Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317, 1083–1086 (2007)
    Article ADS CAS Google Scholar
  9. Pascual, O. et al. Astrocytic purinergic signaling coordinates synaptic networks. Science 310, 113–116 (2005)
    Article ADS CAS Google Scholar
  10. Bezzi, P. et al. CXCR4-activated astrocyte glutamate release via TNFα: amplification by microglia triggers neurotoxicity. Nature Neurosci. 4, 702–710 (2001)
    Article CAS Google Scholar
  11. Stellwagen, D. & Malenka, R. C. Synaptic scaling mediated by glial TNF-α. Nature 440, 1054–1059 (2006)
    Article ADS CAS Google Scholar
  12. Kartvelishvily, E., Shleper, M., Balan, L., Dumin, E. & Wolosker, H. Neuron-derived d-serine release provides a novel means to activate _N_-methyl-d-aspartate receptors. J. Biol. Chem. 281, 14151–14162 (2006)
    Article CAS Google Scholar
  13. Miya, K. et al. Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 510, 641–654 (2008)
    Article CAS Google Scholar
  14. Diamond, J. S., Bergles, D. E. & Jahr, C. E. Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21, 425–433 (1998)
    Article CAS Google Scholar
  15. Luscher, C., Malenka, R. C. & Nicoll, R. A. Monitoring glutamate release during LTP with glial transporter currents. Neuron 21, 435–441 (1998)
    Article CAS Google Scholar
  16. Ge, W. P. & Duan, S. M. Persistent enhancement of neuron–glia signaling mediated by increased extracellular K+ accompanying long-term synaptic potentiation. J. Neurophysiol. 97, 2564–2569 (2007)
    Article CAS Google Scholar
  17. Fiacco, T. A. et al. Selective stimulation of astrocyte calcium in situ does not affect neuronal excitatory synaptic activity. Neuron 54, 611–626 (2007)
    Article CAS Google Scholar
  18. Agulhon, C. et al. What is the role of astrocyte calcium in neurophysiology? Neuron 59, 932–946 (2008)
    Article CAS Google Scholar
  19. Baker, P. F., Knight, D. E. & Umbach, J. A. Calcium clamp of the intracellular environment. Cell Calcium 6, 5–14 (1985)
    Article CAS Google Scholar
  20. Duffy, S., Labrie, V. & Roder, J. C. d-Serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology 33, 1004–1018 (2008)
    Article CAS Google Scholar
  21. Mothet, J. P. et al. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter d-serine. Proc. Natl Acad. Sci. USA 102, 5606–5611 (2005)
    Article ADS CAS Google Scholar
  22. Li, Y., Krupa, B., Kang, J. S., Bolshakov, V. Y. & Liu, G. S. Glycine site of NMDA receptor serves as a spatiotemporal detector of synaptic activity patterns. J. Neurophysiol. 102, 578–589 (2009)
    Article CAS Google Scholar
  23. Fellin, T. et al. Endogenous nonneuronal modulators of synaptic transmission control cortical slow oscillations in vivo . Proc. Natl Acad. Sci. USA 106, 15037–15042 (2009)
    Article ADS CAS Google Scholar
  24. Porter, J. T. & McCarthy, K. D. Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073–5081 (1996)
    Article CAS Google Scholar
  25. Cummings, J. A., Mulkey, R. M., Nicoll, R. A. & Malenka, R. C. Ca2+ signaling requirements for long-term depression in the hippocampus. Neuron 16, 825–833 (1996)
    Article CAS Google Scholar
  26. Strisovsky, K., Jiraskova, J., Mikulova, A., Rulisek, L. & Konvalinka, J. Dual substrate and reaction specificity in mouse serine racemase: Identification of high-affinity dicarboxylate substrate and inhibitors and analysis of the β-eliminase activity. Biochemistry 44, 13091–13100 (2005)
    Article CAS Google Scholar
  27. Bushong, E. A., Martone, M. E., Jones, Y. Z. & Ellisman, M. H. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J. Neurosci. 22, 183–192 (2002)
    Article CAS Google Scholar
  28. Rouach, N., Koulakoff, A., Abudara, V., Willecke, K. & Giaume, C. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322, 1551–1555 (2008)
    Article ADS CAS Google Scholar
  29. Martineau, M., Galli, T., Baux, G. & Mothet, J. P. Confocal imaging and tracking of the exocytotic routes for d-serine-mediated gliotransmission. Glia 56, 1271–1284 (2008)
    Article Google Scholar
  30. Rusakov, D. A. & Kullmann, D. M. Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18, 3158–3170 (1998)
    Article CAS Google Scholar
  31. Bergles, D. E. & Jahr, C. E. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J. Neurosci. 18, 7709–7716 (1998)
    Article CAS Google Scholar
  32. Volterra, A. & Meldolesi, J. Astrocytes, from brain glue to communication elements: the revolution continues. Nature Rev. Neurosci. 6, 626–640 (2005)
    Article CAS Google Scholar
  33. Xu, T., Binz, T., Niemann, H. & Neher, E. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nature Neurosci. 1, 192–200 (1998)
    Article CAS Google Scholar
  34. Szerb, J. C. & Issekutz, B. Increase in the stimulation-induced overflow of glutamate by fluoroacetate, a selective inhibitor of the glial tricarboxylic cycle. Brain Res. 410, 116–120 (1987)
    Article CAS Google Scholar
  35. Rusakov, D. A. & Fine, A. Extracellular Ca2+ depletion contributes to fast activity-dependent modulation of synaptic transmission in the brain. Neuron 37, 287–297 (2003)
    Article CAS Google Scholar
  36. Oertner, T. G., Sabatini, B. L., Nimchinsky, E. A. & Svoboda, K. Facilitation at single synapses probed with optical quantal analysis. Nature Neurosci. 5, 657–664 (2002)
    Article CAS Google Scholar
  37. Scott, R., Ruiz, A., Henneberger, C., Kullmann, D. M. & Rusakov, D. A. Analog modulation of mossy fiber transmission is uncoupled from changes in presynaptic Ca2+ . J. Neurosci. 28, 7765–7773 (2008)
    Article CAS Google Scholar

Download references