Cell-type specific mechanisms of D-serine uptake and release in the brain

Frontiers in Synaptic Neuroscience

Volumn 6, Issue MAY, 2014, Pages

  Martineau, Magalie ^a   Parpura, Vladimir ^b,c   Mothet, Jean Pierre ^d  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b University of Alabama at Birmingham   (United States)

^c University of Rijeka   (Croatia)

^d University of Mediterranée   (France)

Author keywords

Calcium; Coagonists; Exocytosis; NMDA receptors; Synapse; Transporters

Indexed keywords

DEXTRO SERINE;

AMINO ACID TRANSPORT; BRAIN; CELL MEMBRANE; CELL STIMULATION; CELL TYPE; EXTRACELLULAR SPACE; HUMAN; MACROGLIA; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

EID: 84904731795     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2014.00012     Document Type: Review

References (102)

1. Arriza, J. L., Kavanaugh, M. P., Fairman, W. A., Wu, Y. N., Murdoch, G. H., North, R. A., et al. (1993). Cloning and expression of a human neutral amino acid transporter with structural similarity to the glutamate transporter gene family. J. Biol. Chem. 268, 15329-15332.
2. Balan, L., Foltyn, V. N., Zehl, M., Dumin, E., Dikopoltsev, E., Knoh, D., et al. (2009). Feedback inactivation of D-serine synthesis by NMDA receptor-elicited translocation of serine racemase to the membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 7589-7594. doi: 10.1073/pnas.0809442106
3. Balu, D. T., Li, Y., Puhl, M. D., Benneyworth, M. A., Basu, A. C., Takagi, S., et al. (2013). Multiple risk pathways for schizophrenia converge in serine racemase knockout mice, a mouse model of NMDA receptor hypofunction. Proc. Natl. Acad. Sci. U.S.A. 110, E2400-E2409. doi: 10.1073/pnas.1304308110
4. Balu, D. T., and Coyle, J. T. (2012). Neuronal D-serine regulates dendritic architecture in the somatosensory cortex. Neurosci. Lett. 517, 77-81. doi: 10.1016/j.neulet.2012.04.020
5. Balu, D. T., Takagi, S., Puhl, M. D., Benneyworth, M. A., and Coyle, J. T. (2014). D-Serine and serine racemase are localized to neurons in the adult mouse and human forebrain. Cell. Mol. Neurobiol. 34, 419-435. doi: 10.1007/s10571-014-0027-z
6. Bandeira, F., Lent, R., and Herculano-Houzel, S. (2009). Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc. Natl. Acad. Sci. U.S.A. 106, 14108-14113. doi: 10.1073/pnas.0804650106
7. Basu, A. C., Tsai, G. E., Ma, C. L., Ehmsen, J. T., Mustafa, A. K., Han, L., et al. (2009). Targeted disruption of serine racemase affects glutamatergic neurotransmission and behavior. Mol. Psychiatry 14, 719-727. doi: 10.1038/mp.2008.130
8. Benneyworth, M. A., Li, Y., Basu, A. C., Bolshakov, V. Y., and Coyle, J. T. (2012). Cell selective conditional null mutations of serine racemase demonstrate a predominate localization in cortical glutamatergic neurons. Cell. Mol. Neurobiol. 32, 613-624. doi: 10.1007/s10571-012-9808-4
9. Bergersen, L. H., Morland, C., Ormel, L., Rinholm, J. E., Larsson, M., Wold, J. F., et al. (2012). Immunogold detection of L-glutamate and D-serine in small synaptic-like microvesicles in adult hippocampal astrocytes. Cereb. Cortex 22, 1690-1697. doi: 10.1093/cercor/bhr254
10. Bezzi, P., Gundersen, V., Galbete, J. L., Seifert, G., Steinhauser, C., Pilati, E., et al. (2004). Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci. 7, 613-620. doi: 10.1038/nn1246
11. Billard, J. M. (2012). D-Amino acids in brain neurotransmission and synaptic plasticity. Amino Acids 43, 1851-1860. doi: 10.1007/s00726-012-1346-3
12. Bröer, A., Brookes, N., Ganapathy, V., Dimmer, K. S., Wagner, C. A., Lang, F., et al. (1999). The astroglial ASCT2 amino acid transporter as a mediator of glutamine efflux. J. Neurochem. 73, 2184-2194.
13. Campanini, B., Spyrakis, F., Peracchi, A., and Mozzarelli, A. (2013). Serine racemase: a key player in neuron activity and in neuropathologies. Front. Biosci. 18:1112-1128. doi: 10.2741/4167
14. Curcio, L., Podda, M. V., Leone, L., Piacentini, R., Mastrodonato, A., Cappelletti, P., et al. (2013). Reduced D-serine levels in the nucleus accumbens of cocaine-treated rats hinder the induction of NMDA receptor-dependent synaptic plasticity. Brain 136, 1216-1230. doi: 10.1093/brain/awt036
15. DeVito, L. M., Balu, D. T., Kanter, B. R., Lykken, C., Basu, A. C., Coyle, J. T., et al. (2011). Serine racemase deletion disrupts memory for order and alters cortical dendritic morphology. Genes Brain Behav. 10, 210-222. doi: 10.1111/j.1601-183X.2010.00656.x
16. Diniz, L. P., Almeida, J. C., Tortelli, V., Vargas Lopes, C., Setti-Perdigao, P., Stipursky, J., et al. (2012). Astrocyte-induced synaptogenesis is mediated by transforming growth factor beta signaling through modulation of D-serine levels in cerebral cortex neurons. J. Biol. Chem. 287, 41432-41445. doi: 10.1074/jbc.M112.380824
17. Dun, Y., Duplantier, J., Roon, P., Martin, P. M., Ganapathy, V., and Smith, S. B. (2008). Serine racemase expression and D-serine content are developmentally regulated in neuronal ganglion cells of the retina. J. Neurochem. 104, 970-978. doi: 10.1111/j.1471-4159.2007.05015.x
18. Edwards, R. H. (2007). The neurotransmitter cycle and quantal size. Neuron 55, 835-858. doi: 10.1016/j.neuron.2007.09.001
19. Ehmsen, J. T., Ma, T. M., Sason, H., Rosenberg, D., Ogo, T., Furuya, S., et al. (2013). D-serine in glia and neurons derives from 3-phosphoglycerate dehydrogenase. J. Neurosci. 33, 12464-12469. doi: 10.1523/JNEUROSCI.4914-12.2013
20. Eulenburg, V., Armsen, W., Betz, H., and Gomeza, J. (2005). Glycine transporters: essential regulators of neurotransmission. Trends Biochem. Sci. 30, 325-333. doi: 10.1016/j.tibs.2005.04.004
21. Ferraris, D. V., and Tsukamoto, T. (2011). Recent advances in the discovery of D-amino acid oxidase inhibitors and their therapeutic utility in schizophrenia. Curr. Pharm. Des. 17, 103-111. doi: 10.2174/138161211795049633
22. Fossat, P., Turpin, F. R., Sacchi, S., Dulong, J., Shi, T., Rivet, J. M., et al. (2012). Glial D-serine gates NMDA receptors at excitatory synapses in prefrontal cortex. Cereb. Cortex 22, 595-606. doi: 10.1093/cercor/bhr130
23. Fotiadis, D., Kanai, Y., and Palacin, M. (2013). The SLC3 and SLC7 families of amino acid transporters. Mol. Aspects Med. 34, 139-158. doi: 10.1016/j.mam.2012.10.007
24. Fukasawa, Y., Segawa, H., Kim, J. Y., Chairoungdua, A., Kim, D. K., Matsuo, H., et al. (2000). Identification and characterization of a Na(+)-independent neutral amino acid transporter that associates with the 4F2 heavy chain and exhibits substrate selectivity for small neutral D- and L-amino acids. J. Biol. Chem. 275, 9690-9698. doi: 10.1074/jbc.275.13.9690
25. Ge, W. P., Miyawaki, A., Gage, F. H., Jan, Y. N., and Jan, L. Y. (2012). Local generation of glia is a major astrocyte source in postnatal cortex. Nature 484, 376-380. doi: 10.1038/nature10959
26. Gliddon, C. M., Shao, Z., Lemaistre, J. L., and Anderson, C. M. (2009). Cellular distribution of the neutral amino acid transporter subtype ASCT2 in mouse brain. J. Neurochem. 108, 372-383. doi: 10.1111/j.1471-4159.2008.05767.x
27. Hansen, K. B., Ogden, K. K., Yuan, H., and Traynelis, S. F. (2014). Distinct functional and pharmacological properties of triheteromeric GluN1/GluN2A/GluN2B NMDA receptors. Neuron 81, 1084-1096. doi: 10.1016/j.neuron.2014.01.035
28. Harris, K. M., and Sultan, P. (1995). Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34, 1387-1395. doi: 10.1016/0028-3908(95)00142-S
29. Helboe, L., Egebjerg, J., Moller, M., and Thomsen, C. (2003). Distribution and pharmacology of alanine-serine-cysteine transporter 1 (asc-1) in rodent brain. Eur. J. Neurosci. 18, 2227-2238. doi: 10.1046/j.1460-9568.2003.02966.x
30. 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
31. Hikida, T., Mustafa, A. K., Maeda, K., Fujii, K., Barrow, R. K., Saleh, M., et al. (2008). Modulation of D-serine levels in brains of mice lacking PICK1. Biol. Psychiatry 63, 997-1000. doi: 10.1016/j.biopsych.2007.09.025
32. Horio, M., Kohno, M., Fujita, Y., Ishima, T., Inoue, R., Mori, H., et al. (2011). Levels of D-serine in the brain and peripheral organs of serine racemase (Srr) knock-out mice. Neurochem. Int. 59, 853-859. doi: 10.1016/j.neuint.2011.08.017
33. Inoue, R., Hashimoto, K., Harai, T., and Mori, H. (2008). NMDA- and beta-amyloid1-42-induced neurotoxicity is attenuated in serine racemase knock-out mice. J. Neurosci. 28, 14486-14491. doi: 10.1523/JNEUROSCI.5034-08.2008
34. Jahn, R., and Fasshauer, D. (2012). Molecular machines governing exocytosis of synaptic vesicles. Nature 490, 201-207. doi: 10.1038/nature11320
35. Johnson, J. W., and Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531. doi: 10.1038/325529a0
36. Kanai, Y., Clemencon, B., Simonin, A., Leuenberger, M., Lochner, M., Weisstanner, M., et al. (2013). The SLC1 high-affinity glutamate and neutral amino acid transporter family. Mol. Aspects Med. 34, 108-120. doi: 10.1016/j.mam.2013.01.001
37. Kartvelishvily, E., Shleper, M., Balan, L., Dumin, E., and Wolosker, H. (2006). Neuron-derived D-serine release provides a novel means to activate N-methyl-D-aspartate receptors. J. Biol. Chem. 281, 14151-14162. doi: 10.1074/jbc.M512927200
38. Kim, P. M., Aizawa, H., Kim, P. S., Huang, A. S., Wickramasinghe, S. R., Kashani, A. H., et al. (2005). Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. Proc. Natl. Acad. Sci. U.S.A. 102, 2105-2110. doi: 10.1073/pnas.0409723102
39. Kleckner, N. W., and Dingledine, R. (1988). Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837. doi: 10.1126/science.2841759
40. Labrie, V., Duffy, S., Wang, W., Barger, S. W., Baker, G. B., and Roder, J. C. (2008). Genetic inactivation of D-amino acid oxidase enhances extinction and reversal learning in mice. Learn. Mem. 16, 28-37. doi: 10.1101/lm.1112209
41. Li, Y., Sacchi, S., Pollegioni, L., Basu, A. C., Coyle, J. T., and Bolshakov, V. Y. (2013). Identity of endogenous NMDAR glycine site agonist in amygdala is determined by synaptic activity level. Nat. Commun. 4, 1760. doi: 10.1038/ncomms2779
42. Lin, H., Hsu, F. C., Baumann, B. H., Coulter, D. A., and Lynch, D. R. (2014). Cortical synaptic NMDA receptor deficits in alpha7 nicotinic acetylcholine receptor gene deletion models: implications for neuropsychiatric diseases. Neurobiol. Dis. 63, 129-140. doi: 10.1016/j.nbd.2013.11.021
43. Liu, L., Wong, T. P., Pozza, M. F., Lingenhoehl, K., Wang, Y., Sheng, M., et al. (2004). Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304, 1021-1024. doi: 10.1126/science.1096615
44. López-Hidalgo, M., Salgado-Puga, K., Alvarado-Martinez, R., Medina, A. C., Prado-Alcala, R. A., and Garcia-Colunga, J. (2012). Nicotine uses neuron-glia communication to enhance hippocampal synaptic transmission and long-term memory. PLoS ONE 7:e49998. doi: 10.1371/journal.pone.0049998
45. Ma, T. M., Abazyan, S., Abazyan, B., Nomura, J., Yang, C., Seshadri, S., et al. (2013). Pathogenic disruption of DISC1-serine racemase binding elicits schizophrenia-like behavior via D-serine depletion. Mol. Psychiatry 18, 557-567 doi: 10.1038/mp.2012.97
46. Malarkey, E. B., and Parpura, V. (2011). Temporal characteristics of vesicular fusion in astrocytes: examination of synaptobrevin 2 laden vesicles at single vesicle resolution. J. Physiol. 589, 4271-4300. doi: 10.1113/jphysiol.2011.210435
47. Marchaland, J., Cali, C., Voglmaier, S. M., Li, H., Regazzi, R., Edwards, R. H., et al. (2008). Fast subplasma membrane Ca2+ transients control exo-endocytosis of synaptic-like microvesicles in astrocytes. J. Neurosci. 28, 9122-9132. doi: 10.1523/JNEUROSCI.0040-08.2008
48. Martineau, M., Baux, G., and Mothet, J. P. (2006). D-serine signalling in the brain: friend and foe. Trends Neurosci. 29, 481-491. doi: 10.1016/j.tins.2006.06.008
49. Martineau, M., Galli, T., Baux, G., and Mothet, J. P. (2008). Confocal imaging and tracking of the exocytotic routes for D-serine-mediated gliotransmission. Glia 56, 1271-1284. doi: 10.1002/glia.20696
50. Martineau, M., Shi, T., Puyal, J., Knolhoff, A. M., Dulong, J., Gasnier, B., et al. (2013). Storage and uptake of D-serine into astrocytic synaptic-like vesicles specify gliotransmission. J. Neurosci. 33, 3413-3423. doi: 10.1523/JNEUROSCI.3497-12.2013
51. Matsuo, H., Kanai, Y., Tokunaga, M., Nakata, T., Chairoungdua, A., Ishimine, H., et al. (2004). High affinity D- and L -serine transporter Asc-1: cloning and dendritic localization in the rat cerebral and cerebellar cortices. Neurosci. Lett. 358, 123-126. doi: 10.1016/j.neulet.2004.01.014
52. Maucler, C., Pernot, P., Vasylieva, N., Pollegioni, L., and Marinesco, S. (2013). In vivo D-serine hetero-exchange through alanine-serine-cysteine (ASC) transporters detected by microelectrode biosensors. ACS Chem. Neurosci. 4, 772-781. doi: 10.1021/cn4000549
53. Mitchell, J., Paul, P., Chen, H. J., Morris, A., Payling, M., Falchi, M., et al. (2010). Familial amyotrophic lateral sclerosis is associated with a mutation in D-amino acid oxidase. Proc. Natl. Acad. Sci. U.S.A. 107, 7556-7561. doi: 10.1073/pnas.0914128107
54. Miya, K., Inoue, R., Takata, Y., Abe, M., Natsume, R., Sakimura, K., et al. (2008). Serine racemase is predominantly localized in neurons in mouse brain. J. Comp. Neurol. 510, 641-654. doi: 10.1002/cne.21822
55. Montana, V., Malarkey, E. B., Verderio, C., Matteoli, M., and Parpura, V. (2006). Vesicular transmitter release from astrocytes. Glia 54, 700-715. doi: 10.1002/glia.20367
56. Mothet, J. P., Parent, A. T., Wolosker, H., Brady, R. O. Jr., Linden, D. J., et al. (2000). D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc. Natl. Acad. Sci. U.S.A. 97, 4926-4931. doi: 10.1073/pnas.97.9.4926
57. Mothet, J. P., Pollegioni, L., Ouanounou, G., Martineau, M., Fossier, P., and Baux, G. (2005). Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc. Natl. Acad. Sci. U.S.A. 102, 5606-5611. doi: 10.1073/pnas.0408483102
58. Mustafa, A. K., Kumar, M., Selvakumar, B., Ho, G. P., Ehmsen, J. T., Barrow, R. K., et al. (2007). Nitric oxide S-nitrosylates serine racemase, mediating feedback inhibition of D-serine formation. Proc. Natl. Acad. Sci. U.S.A. 104, 2950-2955. doi: 10.1073/pnas.0611620104
59. Mustafa, A. K., Van Rossum, D. B., Patterson, R. L., Maag, D., Ehmsen, J. T., Gazi, S. K., et al. (2009). Glutamatergic regulation of serine racemase via reversal of PIP2 inhibition. Proc. Natl. Acad. Sci. U.S.A. 106, 2921-2926. doi: 10.1073/pnas.0813105106
60. Nakauchi, J., Matsuo, H., Kim, D. K., Goto, A., Chairoungdua, A., Cha, S. H., et al. (2000). Cloning and characterization of a human brain Na(+)-independent transporter for small neutral amino acids that transports D-serine with high affinity. Neurosci. Lett. 287, 231-235. doi: 10.1016/S0304-3940(00)01169-1
61. Panatier, A., Theodosis, D. T., Mothet, J. P., Touquet, B., Pollegioni, L., Poulain, D. A., et al. (2006). Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell 125, 775-784. doi: 10.1016/j.cell.2006.02.051
62. Panizzutti, R., Scoriels, L., and Avellar, M. (2014). The co-agonist site of NMDA-Glutamate receptors: a novel therapeutic target for age-related cognitive decline. Curr. Pharm. Des. doi: 10.2174/1381612819666140110121139 [Epub ahead of print].
63. Paoletti, P., Bellone, C., and Zhou, Q. (2013). NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 14, 383-400. doi: 10.1038/nrn3504
64. Papouin, T., Ladepeche, L., Ruel, J., Sacchi, S., Labasque, M., Hanini, M., et al. (2012). Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633-646. doi: 10.1016/j.cell.2012.06.029
65. Parnis, J., Montana, V., Delgado-Martinez, I., Matyash, V., Parpura, V., Kettenmann, H., et al. (2013). Mitochondrial exchanger NCLX plays a major role in the intracellular Ca2+ signaling, gliotransmission, and proliferation of astrocytes. J. Neurosci. 33, 7206-7219. doi: 10.1523/JNEUROSCI.5721-12.2013
66. Puyal, J., Martineau, M., Mothet, J. P., Nicolas, M. T., and Raymond, J. (2006). Changes in D-serine levels and localization during postnatal development of the rat vestibular nuclei. J. Comp. Neurol. 497, 610-621. doi: 10.1002/cne.21016
67. Reyes, R. C., and Parpura, V. (2008). Mitochondria modulate Ca2+-dependent glutamate release from rat cortical astrocytes. J. Neurosci. 28, 9682-9691. doi: 10.1523/JNEUROSCI.3484-08.2008
68. Reyes, R. C., Perry, G., Lesort, M., and Parpura, V. (2011). Immunophilin deficiency augments Ca2+-dependent glutamate release from mouse cortical astrocytes. Cell Calcium 49, 23-34. doi: 10.1016/j.ceca.2010.11.005
69. Ribeiro, C. S., Reis, M., Panizzutti, R., De Miranda, J., and Wolosker, H. (2002). Glial transport of the neuromodulator D-serine. Brain Res. 929, 202-209. doi: 10.1016/S0006-8993(01)03390-X
70. Rosenberg, D., Artoul, S., Segal, A. C., Kolodney, G., Radzishevsky, I., Dikopoltsev, E., et al. (2013). Neuronal D-serine and glycine release via the Asc-1 transporter regulates NMDA receptor-dependent synaptic activity. J. Neurosci. 33, 3533-3544. doi: 10.1523/JNEUROSCI.3836-12.2013
71. Rosenberg, D., Kartvelishvily, E., Shleper, M., Klinker, C. M., Bowser, M. T., and Wolosker, H. (2010). Neuronal release of D-serine: a physiological pathway controlling extracellular D-serine concentration. FASEB J. 24, 2951-2961. doi: 10.1096/fj.09-147967
72. Rutter, A. R., Fradley, R. L., Garrett, E. M., Chapman, K. L., Lawrence, J. M., Rosahl, T. W., et al. (2007). Evidence from gene knockout studies implicates Asc-1 as the primary transporter mediating d-serine reuptake in the mouse CNS. Eur. J. Neurosci. 25, 1757-1766. doi: 10.1111/j.1460-9568.2007.05446.x
73. Sacchi, S., Caldinelli, L., Cappelletti, P., Pollegioni, L., and Molla, G. (2012). Structure-function relationships in human D-amino acid oxidase. Amino Acids 43, 1833-1850. doi: 10.1007/s00726-012-1345-4
74. Sasabe, J., Miyoshi, Y., Suzuki, M., Mita, M., Konno, R., Matsuoka, M., et al. (2012). D-amino acid oxidase controls motoneuron degeneration through D-serine. Proc. Natl. Acad. Sci. U.S.A. 109, 627-632. doi: 10.1073/pnas.1114639109
75. Schell, M. J., Brady, R. O. Jr., Molliver, M. E., and Snyder, S. H. (1997). D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J. Neurosci. 17, 1604-1615.
76. Schell, M. J., Molliver, M. E., and Snyder, S. H. (1995). D-serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc. Natl. Acad. Sci. U.S.A. 92, 3948-3952. doi: 10.1073/pnas.92.9.3948
77. Scianni, M., Antonilli, L., Chece, G., Cristalli, G., Di Castro, M. A., Limatola, C., et al. (2013). Fractalkine (CX3CL1) enhances hippocampal N-methyl-D-aspartate receptor (NMDAR) function via D-serine and adenosine receptor type A2 (A2AR) activity. J. Neuroinflammation 10, 1742-2094. doi: 10.1186/1742-2094-10-108
78. Shafqat, S., Tamarappoo, B. K., Kilberg, M. S., Puranam, R. S., Mcnamara, J. O., Guadano-Ferraz, A., et al. (1993). Cloning and expression of a novel Na(+)-dependent neutral amino acid transporter structurally related to mammalian Na+/glutamate cotransporters. J. Biol. Chem. 268, 15351-15355.
79. Shao, Z., Kamboj, A., and Anderson, C. M. (2009). Functional and immunocytochemical characterization of D-serine transporters in cortical neuron and astrocyte cultures. J. Neurosci. Res. 87, 2520-2530. doi: 10.1002/jnr.22086
80. Shigetomi, E., Jackson-Weaver, O., Huckstepp, R. T., O'Dell, T. J., and Khakh, B. S. (2013). TRPA1 channels are regulators of astrocyte basal calcium levels and long-term potentiation via constitutive D-serine release. J. Neurosci. 33, 10143-10153. doi: 10.1523/JNEUROSCI.5779-12.2013
81. Singh, P., Jorgacevski, J., Kreft, M., Grubišic, V., Stout, R. F. Jr., Potokar, M., et al. (2014). Single-vesicle architecture of synaptobrevin2 in astrocytes. Nat. Commun. 5:3780. doi: 10.1038/ncomms4780
82. Soares, C., and Lee, K. F. (2013). A prominent role for triheteromeric GluN1/GluN2A/GluN2B NMDARs at central synapses. J. Neurosci. 33, 14975-14977. doi: 10.1523/JNEUROSCI.3109-13.2013
83. Stehberg, J., Moraga-Amaro, R., Salazar, C., Becerra, A., Echeverria, C., Orellana, J. A., et al. (2012). Release of gliotransmitters through astroglial connexin 43 hemichannels is necessary for fear memory consolidation in the basolateral amygdala. FASEB J. 26, 3649-3657. doi: 10.1096/fj.11-198416
84. Takata, N., Mishima, T., Hisatsune, C., Nagai, T., Ebisui, E., Mikoshiba, K., et al. (2011). Astrocyte calcium signaling transforms cholinergic modulation to cortical plasticity in vivo. J. Neurosci. 31, 18155-18165. doi: 10.1523/JNEUROSCI.5289-11.2011
85. Traynelis, S. F., Wollmuth, L. P., Mcbain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., et al. (2010). Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496. doi: 10.1124/pr.109.002451
86. Utsunomiya-Tate, N., Endou, H., and Kanai, Y. (1996). Cloning and functional characterization of a system ASC-like Na+-dependent neutral amino acid transporter. J. Biol. Chem. 271, 14883-14890. doi: 10.1074/jbc.271.25.14883
87. Van Horn, M. R., Sild, M., and Ruthazer, E. S. (2013). D-serine as a gliotransmitter and its roles in brain development and disease. Front. Cell. Neurosci. 7:39. doi: 10.3389/fncel.2013.00039
88. Weiss, M. D., Derazi, S., Kilberg, M. S., and Anderson, K. J. (2001). Ontogeny and localization of the neutral amino acid transporter ASCT1 in rat brain. Brain Res. Dev. Brain Res. 130, 183-190. doi: 10.1016/S0165-3806(01)00250-4
89. Wilhelm, A., Volknandt, W., Langer, D., Nolte, C., Kettenmann, H., and Zimmermann, H. (2004). Localization of SNARE proteins and secretory organelle proteins in astrocytes in vitro and in situ. Neurosci. Res. 48, 249-257. doi: 10.1016/j.neures.2003.11.002
90. Williams, S. M., Diaz, C. M., Macnab, L. T., Sullivan, R. K., and Pow, D. V. (2006). Immunocytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia 53, 401-411. doi: 10.1002/glia.20300
91. Wolosker, H. (2011). Serine racemase and the serine shuttle between neurons and astrocytes. Biochim. Biophys. Acta 1814, 1558-1566. doi: 10.1016/j.bbapap.2011.01.001
92. Wolosker, H., Blackshaw, S., and Snyder, S. H. (1999). Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission. Proc. Natl. Acad. Sci. U.S.A. 96, 13409-13414. doi: 10.1073/pnas.96.23.13409
93. Wolosker, H., Dumin, E., Balan, L., and Foltyn, V. N. (2008). D-amino acids in the brain: D-serine in neurotransmission and neurodegeneration. FEBS J. 275, 3514-3526. doi: 10.1111/j.1742-4658.2008.06515.x
94. Xie, X., Dumas, T., Tang, L., Brennan, T., Reeder, T., Thomas, W., et al. (2005). Lack of the alanine-serine-cysteine transporter 1 causes tremors, seizures, and early postnatal death in mice. Brain Res. 1052, 212-221. doi: 10.1016/j.brainres.2005.06.039
95. Yamamoto, T., Nishizaki, I., Furuya, S., Hirabayashi, Y., Takahashi, K., Okuyama, S., et al. (2003). Characterization of rapid and high-affinity uptake of L-serine in neurons and astrocytes in primary culture. FEBS Lett. 548, 69-73. doi: 10.1016/S0014-5793(03)00742-7
96. Yamamoto, T., Nishizaki, I., Nukada, T., Kamegaya, E., Furuya, S., Hirabayashi, Y., et al. (2004). Functional identification of ASCT1 neutral amino acid transporter as the predominant system for the uptake of L-serine in rat neurons in primary culture. Neurosci. Res. 49, 101-111. doi: 10.1016/j.neures.2004.02.004
97. Yamasaki, M., Yamada, K., Furuya, S., Mitoma, J., Hirabayashi, Y., and Watanabe, M. (2001). 3-Phosphoglycerate dehydrogenase, a key enzyme for L-serine biosynthesis, is preferentially expressed in the radial glia/astrocyte lineage and olfactory ensheathing glia in the mouse brain. J. Neurosci. 21, 7691-7704.
98. Yang, J. H., Wada, A., Yoshida, K., Miyoshi, Y., Sayano, T., Esaki, K., et al. (2010). Brain-specific Phgdh deletion reveals a pivotal role for L-serine biosynthesis in controlling the level of D-serine, an N-methyl-D-aspartate receptor co-agonist, in adult brain. J. Biol. Chem. 285, 41380-41390. doi: 10.1074/jbc.M110.187443
99. Yang, Y., Ge, W., Chen, Y., Zhang, Z., Shen, W., Wu, C., et al. (2003). Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc. Natl. Acad. Sci. U.S.A. 100, 15194-15199. doi: 10.1073/pnas.2431073100
100. Yang, Y., Higashimori, H., and Morel, L. (2013). Developmental maturation of astrocytes and pathogenesis of neurodevelopmental disorders. J. Neurodev. Disord. 5:22. doi: 10.1186/1866-1955-5-22
101. Zhuang, Z., Yang, B., Theus, M. H., Sick, J. T., Bethea, J. R., Sick, T. J., et al. (2010). EphrinBs regulate D-serine synthesis and release in astrocytes. J. Neurosci. 30, 16015-16024. doi: 10.1523/JNEUROSCI.0481-10.2010
102. Zorec, R., Araque, A., Carmignoto, G., Haydon, P. G., Verkhratsky, A., and Parpura, V. (2012). Astroglial excitability and gliotransmission: an appraisal of Ca2+ as a signalling route. ASN Neuro 4, e00080. doi: 10.1042/AN20110061