D-serine signalling as a prominent determinant of neuronal-glial dialogue in the healthy and diseased brain

Journal of Cellular and Molecular Medicine

Volumn 12, Issue 5B, 2008, Pages 1872-1884

  Billard, J M ^a,b,c  

^a CENTRE DE PSYCHIATRIE ET NEUROSCIENCES   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CENTRE PAUL BROCA   (France)

Author keywords

Aging; Alzheimer's disease; Astrocytes; D amino acid; Glutamate; N methyl D aspartate receptors; Neuronal glial communication; Schizophrenia; Synaptic plasticity

Indexed keywords

SERINE;

AGING; ANIMAL; BIOLOGICAL MODEL; BRAIN; BRAIN DISEASE; CHEMISTRY; GLIA; HUMAN; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

AGING; ANIMALS; BRAIN; BRAIN DISEASES; HUMANS; MODELS, NEUROLOGICAL; NEUROGLIA; NEURONS; SERINE; SIGNAL TRANSDUCTION;

EID: 55149085415     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00315.x     Document Type: Review

References (143)

1. Anderson CM, Nedergaard M. Astrocyte-mediated control of cerebral microcircula-tion. Trends Neurosci. 2003 26 : 340 4.
2. Zhou M, Kimelberg HK. Freshly isolated hippocampal CA1 astrocytes comprise two populations differing in glutamate transporter and AMPA receptor expression. J Neurosci. 2001 21 : 7901 8.
3. Bordey A, Sontheimer H. Postnatal development of ionic currents in rat hippocam-pal astrocytes in situ. J Neurophysiol. 1997 78 : 461 77.
4. Sontheimer H, Waxman SG. Expression of voltage-activated ion channels by astrocytes and oligodendrocytes in the hippocampal slice. J Neurophysiol. 1993 70 : 1863 73.
5. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. 1990 247 : 470 3.
6. Dani JW, Chernjavsky A, Smith SJ. Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron. 1992 8 : 429 40.
7. Pasti L, Volterra A, Pozzan T, Carmignoto G. Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci. 1997 17 : 7817 30.
8. Haydon PG. GLIA: listening and talking to the synapse. Nat Rev Neurosci. 2001 2 : 185 93.
9. Angulo MC, Kozlov AS, Charpak S, Audinat E. Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J Neurosci. 2004 24 : 6920 7.
10. Auld DS, Robitaille R. Glial cells and neurotransmission: an inclusive view of synaptic function. Neuron. 2003 40 : 389 400.
11. Newman EA. New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 2003 26 : 536 42.
12. Verkhratsky A, Toescu EC. Neuronal-glial networks as substrate for CNS integration. J Cell Mol Med. 2006 10 : 826 36.
13. Halassa MM, Fellin T, Haydon PG. The tripartite synapse: roles for gliotransmission in health and disease. Trends Mol Med. 2007 13 : 54 63.
14. Seifert G, Schilling K, Steinhauser C. Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat Rev Neurosci. 2006 7 : 194 206.
15. Miller RF. D-Serine as a glial modulator of nerve cells. Glia. 2004 47 : 275 83.
16. Mustafa AK, Kim PM, Snyder SH. D-Serine as a putative glial neurotransmitter. Neuron Glia Biol. 2004 1 : 275 81.
17. Oliet SH, Mothet JP. Molecular determinants of D-serine-mediated gliotransmis-sion: from release to function. Glia. 2006 54 : 726 37.
18. Perea G, Araque A. Glial calcium signaling and neuron-glia communication. Cell Calcium. 2005 38 : 375 82.
19. Corrigan JJ. D-amino acids in animals. Science. 1969 164 : 142 9.
20. Smith JL, Higuchi K. Studies on the nutrition and physiology of Pasteurella pestis. V. Inhibition of growth by D-serine and its reversal by various compounds. J Bacteriol. 1960 79 : 539 43.
21. Whitney JG, Grula EA. A major attachment site for D-serine in the cell wall mucopep-tide of Micrococcus lysodeikticus. Biochim Biophys Acta. 1968 158 : 124 9.
22. Drejer J, Larsson OM, Schousboe A. Characterization of uptake and release processes for D- and L-aspartate in primary cultures of astrocytes and cerebellar granule cells. Neurochem Res. 1983 8 : 231 43.
23. Dunlop DS, Neidle A, McHale D, Dunlop DM, Lajtha A. The presence of free D-aspartic acid in rodents and man. Biochem Biophys Res Commun. 1986 141 : 27 32.
24. nd. D-aspartate in human brain. J Neurochem. 1987 48 : 510 5.
25. Hashimoto A, Nishikawa T, Oka T, Takahashi K. Endogenous D-serine in rat brain: N-methyl-D-aspartate receptor-related distribution and aging. J Neurochem. 1993 60 : 783 6.
26. Hashimoto A, Oka T, Nishikawa T. Extracellular concentration of endogenous free D-serine in the rat brain as revealed by in vivo microdialysis. Neuroscience. 1995 66 : 635 43.
27. Hashimoto A, Oka T, Nishikawa T. Anatomical distribution and postnatal changes in endogenous free D-aspartate and D-serine in rat brain and periphery. Eur J Neurosci. 1995 7 : 1657 63.
28. Schell MJ, Brady RO Jr., Molliver ME, Snyder SH. D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J Neurosci. 1997 17 : 1604 15.
29. Johnson JW, Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature. 1987 325 : 529 31.
30. Verdoorn TA, Kleckner NW, Dingledine R. Rat brain N-methyl-D-aspartate receptors expressed in Xenopus oocytes. Science. 1987 238 : 1114 6.
31. Schell MJ, Molliver ME, Snyder SH. D-serine, an endogenous synaptic modulator: localization to astrocytes and gluta-mate-stimulated release. Proc Natl Acad Sci USA. 1995 92 : 3948 52.
32. Williams SM, Diaz CM, Macnab LT, Sullivan RK, Pow DV. Immuno-cytochemical analysis of D-serine distribution in the mammalian brain reveals novel anatomical compartmentalizations in glia and neurons. Glia. 2006 53 : 401 11.
33. Yamada K, Watanabe M. Cytodifferentiation of Bergmann glia and its relationship with Purkinje cells. Anat Sci Int. 2002 77 : 94 108.
34. 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. 2006 281 : 14151 62.
35. Wu SZ, Bodles AM, Porter MM, Griffin WS, Basile AS, Barger SW. Induction of serine racemase expression and D-serine release from microglia by amyloid beta-peptide. J Neuroinflammation. 2004 1 : 2.
36. Yasuda E, Ma N, Semba R. Immunohistochemical evidences for localization and production of D-serine in some neurons in the rat brain. Neurosci Lett. 2001 299 : 162 4.
37. Wu S, Basile AS, Barger SW. Induction of serine racemase expression and D-serine release from microglia by secreted amyloid precursor protein (sAPP). Curr Alzheimer Res. 2007 4 : 243 51.
38. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P, Baux G. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci USA. 2005 102 : 5606 11.
39. Dunlop DS, Neidle A. The origin and turnover of D-serine in brain. Biochem Biophys Res Commun. 1997 235 : 26 30.
40. Takahashi K, Hayashi F, Nishikawa T. In vivo evidence for the link between L- and D-serine metabolism in rat cerebral cortex. J Neurochem. 1997 69 : 1286 90.
41. Wolosker H, Blackshaw S, Snyder SH. Serine racemase: a glial enzyme synthesizing D-serine to regulate glutamate-N-methyl-D-aspartate neurotransmission. Proc Natl Acad Sci USA. 1999 96 : 13409 14.
42. Wolosker H, Sheth KN, Takahashi M, Mothet J-P, Brady RO Jr., Ferris CD, Snyder SH. Purification of serine race-mase: biosynthesis of the neuromodulator D-serine. Proc Natl Acad Sci USA. 1999 96 : 721 5.
43. De Miranda J, Santoro A, Engelender S, Wolosker H. Human serine racemase: molecular cloning, genomic organization and functional analysis. Gene. 2000 256 : 183 8.
44. Verrall L, Walker M, Rawlings N, Benzel I, Kew JN, Harrison PJ, Burnet PW. D-amino acid oxidase and serine racemase in human brain: normal distribution and altered expression in schizophrenia. Eur J Neurosci. 2007 26 : 1657 69.
45. Xia M, Liu Y, Figueroa DJ, Chiu CS, Wei N, Lawlor AM, Lu P, Sur C, Koblan KS, Connoly TM. Characterization and localization of a human serine racemase. Mol Brain Res. 2004 125 : 96 104.
46. Yamada K, Ohnishi T, Hashimoto K, Ohba H, Iwayama-Shigeno Y, Toyoshima M, Okuno A, Takao H, Toyota T, Minabe Y, Nakamura K, Shimizu E, Itokawa M, Mori N, Iyo M, Yoshikawa T. Identification of multiple serine racemase (SRR) mRNA isoforms and genetic analyses of SRR and DAO in schizophrenia and D-serine levels. Biol Psychiatry. 2005 57 : 1493 503.
47. Yoshikawa M, Takayasu N, Hashimoto A, Sato Y, Tamaki R, Tsukamoto H, Kobayashi H, Noda S. The serine racemase mRNA is predominantly expressed in rat brain neurons. Arch Histol Cytol. 2007 70 : 127 34.
48. Wolosker H. NMDA receptor regulation by D-serine: new findings and perspectives. Mol Neurobiol. 2007 36 : 152 64.
49. Martineau M, Baux G, Mothet JP. D-ser-ine signalling in the brain: friend and foe. Trends Neurosci. 2006 29 : 481 91.
50. De Miranda J, Panizzutti R, Foltyn VN, Wolosker H. Cofactors of serine racemase that physiologically stimulate the synthesis of the N-methyl-D-aspartate (NMDA) receptor coagonist D-serine. Proc Natl Acad Sci USA. 2002 99 : 14542 7.
51. Cook SP, Galve-Roperh I, Martinez del Pozo A, Rodriguez-Crespo I. Direct calcium binding results in activation of brain serine racemase. J Biol Chem. 2002 277 : 27782 92.
52. Shoji K, Mariotto S, Ciampa AR, Suzuki H. Regulation of serine racemase activity by D-serine and nitric oxide in human glioblastoma cells. Neurosci Lett. 2006 392 : 75 8.
53. Dunlop DS, Neidle A. Regulation of serine racemase activity by amino acids. Mol Brain Res. 2005 133 : 208 14.
54. Mustafa AK, Kumar M, Selvakumar B, Ho GP, Ehmsen JT, Barrow RK, Amzel LM, Snyder SH. Nitric oxide S-nitrosylates serine racemase, mediating feedback inhibition of D-serine formation. Proc Natl Acad Sci USA. 2007 104 : 2950 5.
55. Kim PM, Aizawa H, Kim PS, Huang AS, Wickramasinghe SR, Kashani AH, Barrow RK, Huganir RL, Ghosh A, Snyder SH. Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. Proc Natl Acad Sci USA. 2005 102 : 2105 10.
56. Baumgart F, Mancheno JM, Rodriguez-Crespo I. Insights into the activation of brain serine racemase by the multi-PDZ domain glutamate receptor interacting protein, divalent cations and ATP. FEBS J. 2007 274 : 4561 71.
57. Fujii K, Maeda K, Hikida T, Mustafa AK, Balkissoon R, Xia J, Yamada T, Ozeki Y, Kawahara R, Okawa M, Huganir RL, Ujike H, Snyder SH, Sawa A. Serine race-mase binds to PICK1: potential relevance to schizophrenia. Mol Psychiatry. 2006 11 : 150 7.
58. Staudinger J, Lu J, Olson EN. Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-alpha. J Biol Chem. 1997 272 : 32019 24.
59. Hikida T, Mustafa AK, Maeda K, Fujii K, Barrow RK, Saleh M, Huganir RL, Snyder SH, Hashimoto K, Sawa A. Modulation of D-serine levels in brains of mice lacking PICK1. Biol Psychiatry. 2008 63 : 997 1000.
60. Hershko A, Heller H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem Biophys Res Commun. 1985 128 : 1079 86.
61. Dumin E, Bendikov I, Foltyn VN, Misumi Y, Ikehara Y, Kartvelishvily E, Wolosker H. Modulation of D-serine levels via ubiq-uitin-dependent proteasomal degradation of serine racemase. J Biol Chem. 2006 281 : 20291 302.
62. Ciriacks CM, Bowser MT. Measuring the effect of glutamate receptor agonists on extracellular D-serine concentrations in the rat striatum using online microdialysis-capillary electrophoresis. Neurosci Lett. 2006 393 : 200 5.
63. Hashimoto A, Kanda J, Oka T. Effects of N-methyl-D-aspartate, kainate or veratridine on extracellular concentrations of free D-serine and L-glutamate in rat striatum: an in vivo microdialysis study. Brain Res Bull. 2000 53 : 347 51.
64. Bezzi P, Gundersen V, Galbete JL, Seifert G, Steinhauser C, Pilati E, Volterra A. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat Neurosci. 2004 7 : 613 20.
65. Xu J, Peng H, Kang N, Zhao Z, Lin JH, Stanton PK, Kang J. Glutamate-induced exocytosis of glutamate from astrocytes. J Biol Chem. 2007 282 : 24185 97.
66. Zhang Z, Chen G, Zhou W, Song A, Xu T, Luo Q, Wang W, Gu XS, Duan S. Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol. 2007 9 : 945 53.
67. Volterra A, Meldolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci. 2005 6 : 626 40.
68. Ribeiro CS, Reis M, Panizzutti R, de Miranda J, Wolosker H. Glial transport of the neuromodulator D-serine. Brain Res. 2002 929 : 202 9.
69. Helboe L, Egebjerg J, Moller M, Thomsen C. Distribution and pharmacology of alanine-serine-cysteine transporter 1 (asc-1) in rodent brain. Eur J Neurosci. 2003 18 : 2227 38.
70. Matsuo H, Kanai Y, Tokunaga M, Nakata T, Chairoungdua A, Ishimine H, Tsukada S, Ooigawa H, Nawashiro H, Kobayashi Y, Fukuda J, Endou H. High affinity D- and L-serine transporter Asc-1: cloning and dendritic localization in the rat cerebral and cerebellar cortices. Neurosci Lett. 2004 358 : 123 6.
71. Rutter AR, Fradley RL, Garrett EM, Chapman KL, Lawrence JM, Rosahl TW, Patel S. Evidence from gene knockout studies implicates Asc-1 as the primary transporter mediating D-serine reuptake in the mouse CNS. Eur J Neurosci. 2007 25 : 1757 66.
72. Javitt DC, Balla A, Sershen H. A novel alanine-insensitive D-serine transporter in rat brain synaptosomal membranes. Brain Res. 2002 941 : 146 9.
73. Yamamoto N, Tomita U, Umino A, Nishikawa T. Uptake of D-serine by synaptosomal P2 fraction isolated from rat brain. Synapse. 2001 42 : 84 6.
74. Krebs HA. Metabolism of amino-acids: deamination of amino-acids. Biochem J. 1935 29 : 1620 44.
75. Horiike K, Tojo H, Arai R, Nozaki M, Maeda T. D-amino-acid oxidase is confined to the lower brain stem and cerebellum in rat brain: regional differentiation of astrocytes. Brain Res. 1994 652 : 297 303.
76. Moreno S, Nardacci R, Cimini A, Ceru MP. Immunocytochemical localization of D-amino acid oxidase in rat brain. J Neurocytol. 1999 28 : 169 85.
77. Urai Y, Jinnouchi O, Kwak KT, Suzue A, Nagahiro S, Fukui K. Gene expression of D-amino acid oxidase in cultured rat astro-cytes: regional and cell type specific expression. Neurosci Lett. 2002 324 : 101 4.
78. Hashimoto A, Nishikawa T, Konno R, Niwa A, Yasumura Y, Oka T, Takahashi K. Free D-serine, D-aspartate and D-alanine in central nervous system and serum in mutant mice lacking D-amino acid oxidase. Neurosci Lett. 1993 152 : 33 6.
79. Morikawa A, Hamase K, Inoue T, Konno R, Niwa A, Zaitsu K. Determination of free D-aspartic acid, D-serine and D-alanine in the brain of mutant mice lacking D-amino acid oxidase activity. J Chromatogr B Biomed Sci Appl. 2001 757 : 119 25.
80. Shoji K, Mariotto S, Ciampa AR, Suzuki H. Mutual regulation between serine and nitric oxide metabolism in human glioblastoma cells. Neurosci Lett. 2006 394 : 163 7.
81. Hamase K, Konno R, Morikawa A, Zaitsu K. Sensitive determination of D-amino acids in mammals and the effect of D-amino-acid oxidase activity on their amounts. Biol Pharm Bull. 2005 28 : 1578 84.
82. Foltyn VN, Bendikov I, De Miranda J, Panizzutti R, Dumin E, Shleper M, Li P, Toney MD, Kartvelishvily E, Wolosker H. Serine racemase modulates intracellular D-serine levels through an alpha,beta-elimination activity. J Biol Chem. 2005 280 : 1754 63.
83. Strisovsky K, Jiraskova J, Barinka C, Majer P, Rojas C, Slusher BS, Konvalinka J. Mouse brain serine racemase catalyzes specific elimination of L-serine to pyruvate. FEBS Lett. 2003 535 : 44 8.
84. 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 beta-eliminase activity. Biochemistry. 2005 44 : 13091 100.
85. Neidle A, Dunlop DS. Allosteric regulation of mouse brain serine racemase. Neurochem Res. 2002 27 : 1719 24.
86. McDonald JW, Penney JB, Johnston MV, Young AB. Characterization and regional distribution of strychnine-insensitive [3H]glycine binding sites in rat brain by quantitative receptor autoradiography. Neuroscience. 1990 35 : 653 68.
87. Matsui T, Sekiguchi M, Hashimoto A, Tomita U, Nishikawa T, Wada K. Functional comparison of D-serine and glycine in rodents: the effect on cloned NMDA receptors and the extracellular concentration. J Neurochem. 1995 65 : 454 8.
88. Mothet JP, Parent AT, Wolosker H, Brady RO Jr., Linden DJ, Ferris CD, Rogawski MA, Snyder SH. D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. Proc Natl Acad Sci USA. 2000 97 : 4926 31.
89. Yang Y, Ge W, Chen Y, Zhang Z, Shen W, Wu C, Poo M, Duan S. Contribution of astrocytes to hippocampal long-term potentiation through release of D-serine. Proc Natl Acad Sci USA. 2003 100 : 15194 9.
90. Panatier A, Theodosis DT, Mothet JP, Touquet B, Pollegioni L, Poulain DA, Oliet SH. Glia-derived D-serine controls NMDA receptor activity and synaptic memory. Cell. 2006 125 : 775 84.
91. Chen L, Muhlhauser M, Yang CR. Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo. J Neurophysiol. 2003 89 : 691 703.
92. Martina M, Gorfinkel Y, Halman S, Lowe JA, Periyalwar P, Schmidt CJ, Bergeron R. Glycine transporter type 1 blockade changes NMDA receptor-mediated responses and LTP in hippocampal CA1 pyramidal cells by altering extracellular glycine levels. J Physiol. 2004 557 : 489 500.
93. Martina M, ME BT, Halman S, Tsai G, Tiberi M, Coyle JT, Bergeron R. Reduced glycine transporter type 1 expression leads to major changes in glutamatergic neuro-transmission of CA1 hippocampal neurones in mice. J Physiol. 2005 563 : 777 93.
94. Martina M, Krasteniakov NV, Bergeron R. D-serine differently modulates NMDA receptor function in rat CA1 hippocampal pyramidal cells and interneurons. J Physiol. 2003 548 : 411 23.
95. Wake K, Yamazaki H, Hanzawa S, Konno R, Sakio H, Niwa A, Hori Y. Exaggerated responses to chronic nociceptive stimuli and enhancement of N-methyl-D-aspartate receptor-mediated synaptic transmission in mutant mice lacking D-amino-acid oxidase. Neurosci Lett. 2001 297 : 25 8.
96. Maekawa M, Watanabe M, Yamaguchi S, Konno R, Hori Y. Spatial learning and long-term potentiation of mutant mice lacking D-amino-acid oxidase. Neurosci Res. 2005 53 : 34 8.
97. Stevens ER, Esguerra M, Kim PM, Newman EA, Snyder SH, Zahs KR, Miller RF. D-serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors. Proc Natl Acad Sci USA. 2003 100 : 6789 94.
98. Gustafson EC, Stevens ER, Wolosker H, Miller RF. Endogenous D-serine contributes to NMDA-receptor-mediated light-evoked responses in the vertebrate retina. J Neurophysiol. 2007 98 : 122 30.
99. Luscher C, Nicoll RA, Malenka RC, Muller D. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci. 2000 3 : 545 50.
100. Martin SJ, Grimwood PD, Morris RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci. 2000 23 : 649 711.
101. Mothet JP, Rouaud E, Sinet PM, Potier B, Jouvenceau A, Dutar P, Videau C, Epelbaum J, Billard JM. A critical role for the glial-derived neuromodulator D-serine in the age-related deficits of cellular mechanisms of learning and memory. Aging Cell. 2006 5 : 267 74.
102. Gong XQ, Zabek RL, Bai D. D-serine inhibits AMPA receptor-mediated current in rat hippocampal neurons. Can J Physiol Pharmacol. 2007 85 : 546 55.
103. Junjaud G, Rouaud E, Turpin F, Mothet JP, Billard JM. Age-related effects of the neuromodulator D-serine on neurotransmission and synaptic potentiation in the CA1 hippocampal area of the rat. J Neurochem. 2006 98 : 1159 66.
104. Krasteniakov NV, Martina M, Bergeron R. Subthreshold contribution of N-methyl-D-aspartate receptors to long-term potentia-tion induced by low-frequency pairing in rat hippocampal CA1 pyramidal cells. Neuroscience. 2004 126 : 83 94.
105. Rouaud E, Billard JM. D-cycloserine facilitates synaptic plasticity but impairs gluta-matergic neurotransmission in rat hippocampal slices. Br J Pharmacol. 2003 140 : 1051 6.
106. Hashimoto A, Chiba S. Effect of systemic administration of D-serine on the levels of D- and L-serine in several brain areas and periphery of rat. Eur J Pharmacol. 2004 495 : 153 8.
107. Naur P, Hansen KB, Kristensen AS, Dravid SM, Pickering DS, Olsen L, Vestergaard B, Egebjerg J, Gajhede M, Traynelis SF, Kastrup JS. Ionotropic glutamate-like receptor delta2 binds D-serine and glycine. Proc Natl Acad Sci USA. 2007 104 : 14116 21.
108. Kashiwabuchi N, Ikeda K, Araki K, Hirano T, Shibuki K, Takayama C, Inoue Y, Kutsuwada T, Yagi T, Kang Y. Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluR delta 2 mutant mice. Cell. 1995 81 : 245 52.
109. Billard JM. Ageing, hippocampal synaptic activity and magnesium. Magnes Res. 2006 19 : 199 215.
110. Barnes CA, Rao G, Shen J. Age-related decrease in the N-methyl-D-aspartateR-mediated excitatory postsynaptic potential in hippocampal region CA1. Neurobiol Aging. 1997 18 : 445 52.
111. Potier B, Poindessous-Jazat F, Dutar P, Billard JM. NMDA receptor activation in the aged rat hippocampus. Exp Gerontol. 2000 35 : 1185 99.
112. Yang S, Qiao H, Wen L, Zhou W, Zhang Y. D-serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci Lett. 2005 379 : 7 12.
113. Miyoshi R, Kito S, Doudou N, Nomoto T. Age-related changes of strychnine-insensitive glycine receptors in rat brain as studied by in vitro autoradiography. Synapse. 1990 6 : 338 43.
114. Nagata Y, Uehara T, Kitamura Y, Nomura Y, Horiike K. D-serine content and D-[3H]serine binding in the brain regions of the senescence-accelerated mouse. Mech Ageing Dev. 1998 104 : 115 24.
115. Aura J, Riekkinen P Jr. Pre-training blocks the improving effect of tetrahydroaminoacridine and D-cycloserine on spatial navigation performance in aged rats. Eur J Pharmacol. 2000 390 : 313 8.
116. Baxter MG, Lanthorn TH, Frick KM, Golski S, Wan RQ, Olton DS. D-cycloser-ine, a novel cognitive enhancer, improves spatial memory in aged rats. Neurobiol Aging. 1994 15 : 207 13.
117. Thompson LT, Disterhoft JF. Age- and dose-dependent facilitation of associative eyeblink conditioning by D-cycloserine in rabbits. Behav Neurosci. 1997 111 : 1303 12.
118. Billard JM, Rouaud E. Deficit of NMDA receptor activation in CA1 hippocampal area of aged rats is rescued by D-cycloserine. Eur J Neurosci. 2007 25 : 2260 8.
119. Krug AW, Volker K, Dantzler WH, Silbernagl S. Why is D-serine nephrotoxic and alpha-aminoisobutyric acid protective? Am J Physiol Renal Physiol. 2007 293 : F382 90.
120. Lewis WC, Calden G, Thurston JR, Gilson WE. Psychiatric and neurological reactions to cycloserine in the treatment of tuberculosis. Dis Chest. 1957 32 : 172 82.
121. Williams RE, Lock EA. D-serine-induced nephrotoxicity: possible interaction with tyrosine metabolism. Toxicology. 2004 201 : 231 8.
122. Tannenberg RK, Scott HL, Westphalen RI, Dodd PR. The identification and characterization of excitotoxic nerve-endings in Alzheimer disease. Curr Alzheimer Res. 2004 1 : 11 25.
123. Lipton SA. The molecular basis of memantine action in Alzheimer's disease and other neurologic disorders: low-affinity, uncompetitive antagonism. Curr Alzheimer Res. 2005 2 : 155 65.
124. Parsons CG, Stoffler A, Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system - too little activation is bad, too much is even worse. Neuropharmacology. 2007 53 : 699 723.
125. Barger SW, Goodwin ME, Porter MM, Beggs ML. Glutamate release from activated microglia requires the oxidative burst and lipid peroxidation. J Neurochem. 2007 101 : 1205 13.
126. Vesce S, Rossi D, Brambilla L, Volterra A. Glutamate release from astrocytes in physiological conditions and in neurode-generative disorders characterized by neuroinflammation. Int Rev Neurobiol. 2007 82 : 57 71.
127. Wu S, Barger SW. Induction of serine racemase by inflammatory stimuli is dependent on AP-1. Ann N Y Acad Sci. 2004 1035 : 133 46.
128. Heese K, Nagai Y, Sawada T. Induction of rat L-phosphoserine phosphatase by amyloiD-beta (1-42) is inhibited by interleukin-11. Neurosci Lett. 2000 288 : 37 40.
129. Katsuki H, Nonaka M, Shirakawa H, Kume T, Akaike A. Endogenous D-serine is involved in induction of neuronal death by N-methyl-D-aspartate and simulated ischemia in rat cerebrocortical slices. J Pharmacol Exp Ther. 2004 311 : 836 44.
130. Shleper M, Kartvelishvily E, Wolosker H. D-serine is the dominant endogenous coagonist for NMDA receptor neurotoxicity in organotypic hippocampal slices. J Neurosci. 2005 25 : 9413 7.
131. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991 30 : 572 80.
132. Toda M, Abi-Dargham A. Dopamine hypothesis of schizophrenia: making sense of it all. Curr Psychiatry Rep. 2007 9 : 329 36.
133. Javitt DC. Glutamate and schizophrenia: phencyclidine, N-methyl-D-aspartate receptors, and dopamine-glutamate interactions. Int Rev Neurobiol. 2007 78 : 69 108.
134. Millan MJ. N-methyl-D-aspartate receptors as a target for improved antipsychotic agents: novel insights and clinical perspectives. Psychopharmacology 2005 179 : 30 53.
135. Coyle JT. Substance use disorders and Schizophrenia: a question of shared glutamatergic mechanisms. Neurotox Res. 2006 10 : 221 33.
136. Bendikov I, Nadri C, Amar S, Panizzutti R, De Miranda J, Wolosker H, Agam G. A CSF and postmortem brain study of D-serine metabolic parameters in schizophrenia. Schizophr Res. 2007 90 : 41 51.
137. Goltsov AY, Loseva JG, Andreeva TV, Grigorenko AP, Abramova LI, Kaleda VG, Orlova VA, Moliaka YK, Rogaev El. Polymorphism in the 5'-promoter region of serine racemase gene in schizophrenia. Mol Psychiatry. 2006 11 : 325 6.
138. Morita Y, Ujike H, Tanaka Y, Otani K, Kishimoto M, Morio A, Kotaka T, Okahisa Y, Matsushita M, Morikawa A, Hamase K, Zaitsu K, Kuroda S. A genetic variant of the serine racemase gene is associated with schizophrenia. Biol Psychiatry. 2007 61 : 1200 3.
139. Boks MP, Rietkerk T, van de Beek MH, Sommer IE, de Koning TJ, Kahn RS. Reviewing the role of the genes G72 and DAAO in glutamate neurotransmission in schizophrenia. Eur Neuropsychopharmacol. 2007 17 : 567 72.
140. Chumakov I, Blumenfeld M, Guerassimenko O, Cavarec L, Palicio M, Abderrahim H, Bougueleret L, Barry C, Tanaka H, La Rosa P, Puech A, Tahri N, Cohen-Akenine A, Delabrosse S, Lissarrague S, Picard FP, Maurice K, Essioux L, Millasseau P, Grel P, Debailleul V, Simon AM, Caterina D, Dufaure I, Malekzadeh K, Belova M, Luan JJ, Bouillot M, Sambucy JL, Primas G, Saumier M, Boubkiri N, Martin-Saumier S, Nasroune M, Peixoto H, Delaye A, Pinchot V, Bastucci M, Guillou S, Chevillon M, Sainz-Fuertes R, Meguenni S, Aurich-Costa J, Cherif D, Gimalac A, Van Duijn C, Gauvreau D, Ouellette G, Fortier I, Raelson J, Sherbatich T, Riazanskaia N, Rogaev E, Raeymaekers P, Aerssens J, Konings F, Luyten W, Macciardi F, Sham PC, Straub RE, Weinberger DR, Cohen N, Cohen D. Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc Natl Acad Sci USA. 2002 99 : 13675 80.
141. Shinkai T, De Luca V, Hwang R, Müller DJ, Lanktree M, Zai G, Shaikh S, Wong G, Sicard T, Potapova N, Trakalo J, King N, Matsumoto C, Hori H, Wong AH, Ohmori O, Macciardi F, Nakamura J, Kennedy JL. Association analyses of the DAOA/G30 and D-amino-acid oxidase genes in schizophrenia: further evidence for a role in schizophrenia. Neuromolecular Med. 2007 9 : 169 77.
142. Konarski JZ, McIntyre RS, Grupp LA, Kennedy SH. Is the cerebellum relevant in the circuitry of neuropsychiatric disorders? J Psychiatry Neurosci. 2005 30 : 178 86.
143. Yoshikawa M, Ito K, Maeda M, Akahori K, Takahashi S, Jin XL, Matsuda M, Suzuki T, Oka T, Kobayashi H, Hashimoto A. Activation of supraspinal NMDA receptors by both D-serine alone or in combination with morphine leads to the potentiation of antinociception in tailflick test of rats. Eur J Pharmacol. 2007 565 : 89 97.