Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo

Journal of Neurophysiology

Volumn 89, Issue 2, 2003, Pages 691-703

  Chen, Long ^a   Muhlhauser, Mark ^a   Yang, Charles R ^a  

^a ELI LILLY AND COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINO 1 HYDROXY 2 PYRROLIDINONE; CARRIER PROTEIN; GLUTAMIC ACID; GLYCINE; GLYCINE TRANSPORTER 1; N [3 (4' FLUOROPHENYL) 3 (4' PHENYLPHENOXY)PROPYL]SARCOSINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN INHIBITOR; SERINE; UNCLASSIFIED DRUG; URETHAN;

AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXTRACELLULAR SPACE; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MALE; MEMBRANE CURRENT; MEMORY; MICROIONTOPHORESIS; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PATHOPHYSIOLOGY; POSTSYNAPTIC MEMBRANE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; RAT; RECEPTOR BINDING; RECEPTOR INTRINSIC ACTIVITY; SCHIZOPHRENIA; SYNAPSE;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; IONTOPHORESIS; MALE; N-METHYLASPARTATE; NEURONS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PYRROLIDINONES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SARCOSINE; SERINE;

EID: 0037320805     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00680.2002     Document Type: Article

References (102)

1. Adam RH, Sato K, Shimada S, Tohyama M, Puschel AW, and Betz H. Gene structure and glial expression of the glycine transporter GlyT1 in embryonic and adult rodents. J Neurosci 15: 2524-2532, 1995.
2. Anson LC, Chen PE, Wyllie DJA, Colquhoun D, and Schoepfer R. Identification of amino acid residues of the NR2A subunit that control glutamate potency in recombinant NR1/NR2A NMDA receptors. J Neurosci 18: 581-589, 1998.
3. Atkinson BN, Bell SC, De Vivo M, Kowalski LR, Lechner SM, Ognyanov VI, Tham CS, Tsai C, Jia J, Ashton D, and Klitenick MA. ALX 5407: a potent, selective inhibitor of the hGlyT1 glycine transporter. Mol Pharmacol 60: 1414-1420, 2001.
4. Aubrey KR and Vandenberg RJ. N[3-(4′-fluorophenyl)-3-(4′-phenylphenoxy)propyl]sarcosine (NFPS) is a selective persistent inhibitor of glycine transport. Br J Pharmacol 134: 1429-1436, 2001.
5. Baranano DE, Ferris CD, and Snyder SH. Atypical neural messengers. Trends Neurosci 24: 99-106, 2001.
6. 3H]MDL-105, 519, a high affinity radioligand for the N-methyl-D-aspartate receptor-associated glycine recognition site. J Pharmacol Exp Ther 279: 62-68, 1996.
7. Bashir ZI, Tam B, and Collingridge GL Activation of the glycine site in the NMDA receptor is necessary for the induction of LTP. Neurosci Lett 108: 261-266, 1990.
8. Benveniste M, Clements J, Vyklicky L Jr, and Mayer ML. A kinetic analysis of the modulation of N-methyl-D-aspartic acid receptors by glycine in mouse cultured hippocampal neurons. J Physiol 428: 333-357, 1990.
9. Berger AJ, Dieudonne S, and Ascher P. Glycine uptake governs glycine site occupancy at NMDA receptors of excitatory synapses. J Neurophysiol 80: 3336-3340, 1998.
10. Bergeron R, Meyer TM, Coyle JT, and Greene RW. Modulation of N-methyl-D-aspartate receptor function by glycine transport. Proc Natl Acad Sci USA 95: 15730-15734, 1998.
11. Bliss TVP and Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39, 1993.
12. Borowsky B and Hoffman BJ. Analysis of a gene encoding two glycine transporter variants reveals alternative promoter usage and a novel gene structure. J Biol Chem 273: 29077-29085, 1998.
13. Borowsky B, Mezey E, and Hoffman BJ. Two glycine transporter variants with distinct localization in the CNS and peripheral tissues are encoded by a common gene. Neuron 10: 851-863, 1993.
14. Breier A. Cognitive deficit in schizophrenia and its neurochemical basis. Br J Psychiatry Suppl 37: 16-18, 1999.
15. Broer A, Brooks N, Ganapathy V, Dimmer KS, Wagner CA, Lang F, and Borer S. The astogial ASCT2 amino acid transporter as a mediator of glutamate efflux. J Neuroschem 73: 2184-2194, 1990.
16. Brugger F, Wicki U, Nassenstein-Elton D, Fagg GE, Olpe HR, and Pozza MF. Modulation of the NMDA receptor by D-serine in the cortex and the spinal cord in vitro. Eur J Pharmacol 191: 29-38, 1990.
17. Carmignoto G and Vicini S Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258: 1007-1011, 1992.
18. Chen L, Muhlhauser M, and Yang CR. Blockade of glycine transporter-1 (GlyT1) augments nmda receptor (nmda-r) mediated neuronal responses in rat prefrontal cortex in vitro and in vivo. Soc Neurosci Abstr 815.14, 2001.
19. Clark GD, Clifford DB, and Zorumski CF. The effect of agonist concentration, membrane voltage and calcium on N-methyl-D-aspartate receptor desensitization. Neuroscience 39: 787-797, 1990.
20. Cull-Candy S, Brickley S, and Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335, 2001.
21. Currás C and Pallotta BS. Single-channel evidence for glycine and NMDA requirement in NMDA receptor activation. Brain Res 740: 27-40, 1996.
22. Czepita D, Daw NW, and Reid SNM. Glycine at the NMDA receptor in cat visual cortex: saturation and changes with age. J Neurophysiol 75: 311-317, 1996.
23. Dalkara T, Erdemli G, Barun S, and Onur R. Glycine is required for NMDA receptor activation: electrophysiological evidence from intact rat hippocampus. Brain Res 576: 197-202, 1992.
24. D'Angelo E, Rossi P, and Garthwaite J. Dual-component NMDA receptor currents at a single central synapse. Nature 346: 467-70, 1990.
25. D'Angelo E, Rossi P, and Taglietti V. Voltage-dependent kinetics of N-methyl-D-aspartate synaptic currents in rat cerebellar granule cells. Eur J Neurosci 6: 640-645, 1994.
26. Danysz W and Parsons CG. Glycine and N-methyl-D-aspartate receptors: physiological significance and possible therapeutic applications. Pharmacol Rev 50: 598-664, 1998.
27. 3H-glycine uptake in rat hippocampus: kinetic analysis and autoradiographic localization. Brain Res 572: 154-163, 1992.
28. Ferraro TN and Hare TA. Free and conjugated amino acids in human CSF: influence of age and sex. Brain Res 338: 53-60, 1985.
29. Foster AC and Kemp JA. HA-966 antagonizes N-methyl-D-aspartate receptors through a selective interaction with the glycine modulatory site. J Neurosci 9: 2191-2196, 1989.
30. Fletcher EJ and Lodge D. Glycine reverses antagonism of N-methyl-D-aspartate (NMDA) by 1-hydroxy-3-aminopyrrolidone-2 (HA-966) but not by D-2-amino-5-phosphonovalerate (D-AP5) on rat cortical slices. Eur J Pharmacol 151: 161-162, 1988.
31. Flint AC, Maisch US, Weishaupt JH, Kriegstein AR, and Monyer H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J Neurosci 17: 2469-2476, 1997.
32. Gibb AJ and Colquhoun D. Glutamate activation of a single NMDA receptor-channel produces a cluster of channel openings. Proc R Soc Lond B Biol Sci 243: 39-45, 1991.
33. Gigg J, Tan AM, and Finch DM. Glutamatergic hippocampal formation projections to prefrontal cortex in the rat are regulated by GABAergic inhibition and show convergence with glutamatergic projections from the limbic thalamus. Hippocampus 4: 189-198, 1994.
34. Goff DC, Tsai G, Levitt J, Amico E, Manoach D, Schoenfeld DA, Hayden DL, McCarley R, and Coyle JT. A placebo-controlled trial of D-cycloserine added to conventional neuroleptics in patients with schizophrenia. Arch Gen Psychiatry 56: 21-27, 1999.
35. Goldman-Rakic PS. The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biol Psychiatry 46: 650-661, 1999.
36. 3H]L-689560, an antagonist for the glycine site on the N-methyl-D-aspartate receptor, to rat brain membrane. Mol Pharamcol 41: 923-930, 1992.
37. Hashimoto A and Oka T. Free D-aspartate and D-serine in the mammalian brain and periphery. Prog Neurobiol 52: 325-353, 1997.
38. Hashimoto A, Oka T, and Nishikawa T. Extracellular concentration of endogenous free D-serine in the rat brain as revealed by in vivo microdialysis. Neuroscience 66: 635-643, 1995.
39. Herdon HJ, Godgrey FM, Brown AM, Coulton S, Evans JR, and Cairns WJ. Pharmacological assessment of the role of the glycine tranporter GlyT-1 in mediating high-affinity glycine uptake by rat cerebral cortex and cerebellum synaptosomes. Neuropharmacology 41: 88-96, 2001.
40. Heresco-Levy U and Javitt DC. The role of N-methyl-D-aspartate (NMDA) receptor-mediated neurotransmission in the pathophysiology and therapeutics of psychiatric syndromes. Eur Neuropsychopharmacol 8: 141-152, 1998.
41. Heresco-Levy U, Javitt DC, Mordel EM, Silipo G, and Lichtenstein M. Efficacy of high-dose glycine in the treatment of enduring negative symptoms of schizophrenia. Arch Gen Psychiatry 56: 29-36, 1999.
42. Hestrin S, Sah P, and Nicoll RA. Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5: 247-253, 1990.
43. Hestrin S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357: 686-689, 1992.
44. Hirai H, Kirsch J, Laube B, Betz H, and Kuhse J. The glycine binding site of the N-methyl-D-aspartate receptor subunit NR1: identification of novel determinants of coagonist potentiation in the extracellular m3-m4 loop region. Proc Natl Acad Sci USA 93: 6031-6036, 1996.
45. Javitt DC, Balla A, Sershen H, and Lajtha A. Reversal of phencyclidineinduced effects by glycine and glycine transport inhibitors. Biol Psychiatry 45: 668-679, 1999.
46. Javitt DC and Zurkin SR. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148: 1301-1308, 1991.
47. Javitt DC, Zylberman I, Zukin S, Heresco-Levy U, and Lindenmayer J-P. Amelioration of negative symptoms in schizophrenia by glycine. Am J Psychiatry 151: 1234-1236, 1994.
48. Johnson JW and Ascher P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325: 529-531, 1987.
49. Kemp JA, Foster AC, Lesson PD, Priestly T, Tridgett R, Iversen LL, and Woodruff GN. 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of the N-methyl-D-aspartate receptor complex. Proc Natl Acad Sci USA 85: 6547-6550, 1988.
50. Kew JNC, Richards JG, Mutel V, and Kemp JA. Developmental changes in NMDA receptor glycine affinity and ifenprodil sensitivity reveal three distinct populations of NMDA receptors in individual rat cortical neurons. J Neurosci 18: 1935-1943, 1998.
51. Kim KM, Kingsmore SF, Han H, Yang-Feng TL, Godinot N, Seldin MF, Caron MG, and Giros B. Cloning of the human glycine transporter type 1: molecular and pharmacological characterization of novel isoform variants and chromosomal localization of the gene in the human and mouse genomes. Mol Pharmacol 45: 608-617, 1994.
52. Kleckner NW and Dingledine R. Requirement for glycine in activation of NMDA receptors expressed in Xenopus oocytes. Science 214: 835-837, 1988.
53. Laube B, Hirai H, Sturgess M, Betz H, and Kuhse J. Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18: 493-503, 1997.
54. Legendre P. The glycinergic inhibitory synapse. Cell Mol Life Sci 58: 760-793, 2001.
55. Legendre P, Rosenmund C, and Westbrook GL. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13: 674-684, 1993.
56. Lerma J, Zukin RS, and Bennett MVL. Glycine decrease desensitization of N-methyl-D-aspartate (NMDA) receptors expressed in Xenopus oocytes and is required for NMDA responses. Proc Natl Acad Sci USA 87: 2354-2358, 1990.
57. Lester RA, Clements JD, Westbrook GL, and Jahr CE. Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents. Nature 346: 565-567, 1990.
58. Lester RA and Jahr CE. NMDA channel behavior depends on agonist affinity. J Neurosci 12: 635-643, 1992.
59. Lester RA, Tong G, and Jahr CE. Interactions between the glycine and glutamate binding sites of the NMDA receptor. J Neurosci 13: 1088-1096, 1993.
60. Malenka RC and Nicoll RA. Long-term potentiation - a decade of progress? Science 285: 1870-1874, 1999.
61. Matsui T-A, Sekiguchi M, Hashimoto A, Tomita U, Nishikawa T, and Wada K. Functional comparison of D-serine and glycine in rodents: the effect on cloned NMDA receptors and the extracellular concentration. J Neurochem 65: 454-458, 1995.
62. 2+ of NMDA responses in spinal cord neurons. Nature 309: 261-263, 1984.
63. Mayer ML, Vyklicky L Jr, and Clements J. Regulation of NMDA receptor desensitization in mouse by glycine. Nature 338: 425-427, 1989.
64. McBain CJ and Mayer ML. N-methyl-D-aspartic acid receptor structure and function. Physiol Rev 74: 723-760, 1994.
65. Mizutani A, Saito H, and Abe K. Evidence for involvement of endogenous glycine in the induction of long-term potentiation in the dentate gyrus of anesthetized rats. Eur J Pharmacol 205: 303-305, 1991.
66. Monyer H, Burnashev N, Laurie DJ, Sakmann B, and Seeburg PH. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
67. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, and Seeburg PH. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256: 1217-1221, 1992.
68. Nowak LM, Bregestovski P, Ascher P, Herbert A, and Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neruons. Nature 307: 462-465, 1984.
69. Oldendorf WH. Stereospecificity of blood-brain barrier permeability to amino acids. Am J Physiol 224: 967-969, 1973.
70. Parsons CG, Danysz W, Hesselink M, Hartmann S, Lorenz B, Wollenburg C, and Quark G. Modulation of NMDA receptors by glycine - introduction to some basic aspects and recent developments. Amino Acids 14: 207-216, 1998.
71. Parsons CG, Gruner R, Rozental J, Millar J, and Lodge D. Patch clamp studies on the kinetics and selectivity of N-methyl-D-aspartate receptor antagonism by memantine (1-amino-3,5-demethyladamantan). Neuroscience 32: 1337-1350, 1993.
72. Patel J, Zinkand WC, Thompson C, and Salama A. Role of gycine in N-methyl-D-aspartate-mediated neuronal cytotoxicity. J Neurochem 54: 849-854, 1990.
73. Paxinos G and Watson C. The Rat Brain in Stereotaxic Coordinates (4th ed.), New York: Academic Press, 1998.
74. Ribeiro CS, Reis M, Panizzutti R, Miranda J de, and Wolosker H. Glial transport of the neuromodulator D-serine. Brain Res 929: 202-209, 2002.
75. Rosenmund C, Feltz A, and Westbrook GL. Calcium-dependent inactivation of synaptic NMDA receptors in hippocampal neurons. J Neurophysiol 73: 427-430, 1995.
76. Sakata K, Sato K, Schloss P, Betz H, Shimada S, and Tohyama M. Characterization of glycine release mediated by glycine tranporter 1 stably expressed in HEK-293 cells. Mol Brain Res 49: 89-94, 1997.
77. Salt TE. Modulation of NMDA receptor-mediated responses by glycine and D-serine in the rat thalamus in vivo. Brain Res 481: 403-406, 1989.
78. Schell MJ, Brady RO Jr, Molliver ME, and Snyder SH. D-Serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J Neurosci 17: 1604-1615, 1997.
79. Schell MJ, Molliver ME, and Snyder SH. D-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci USA 92: 3948-3952, 1995.
80. Schoham S, Javitt DC, and Heresco-Levy U. High dose glycine nutrition effects glial cell morphology in rat hippocampus and cerebellum. Int J Neuropsychopharmacol 2: 35-40, 1999.
81. 2+ channels in the proximal versus distal dendrites to synaptic integration in prefrontal cortical neurons. J Neurosci 17: 5936-5948, 1997.
82. Smith KE, Borden LA, Hartig PR, Branchek T, and Weinshank RL. Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8: 927-935, 1992.
83. Snyder SH and Ferris C. Novel neurotransmitters and their neuropsychiatric relevance. Am J Psychiatry 157: 1738-1751, 2000.
84. Snyder SH and Kim PM. D-Amino acids as putative neurotransmitters: focus on D-serine. Neurochem Res 25: 553-560, 2000.
85. Steinpreis RE. The behavioral and neurochemical effects of phencyclidine in human and animals: some implications for modeling psychosis. Behav Brain Res 74: 45-55, 1996.
86. Supplisson S and Bergman C. Control of NMDA receptor activation by a glycine transporter co-expressed in Xenopus oocytes. J Neurosci 17: 4580-4590, 1997.
87. Tamminga CA. Schizophrenia and glutamatergic transmission. Critical Rev Neurobiol 12: 21-36, 1998.
88. Thomson AM. Glycine is a coagonist at the NMDA receptor channel complex. Prog Neurobiol 35: 53-74, 1990.
89. Tong G, Shepherd D, and Jahr CE. Synaptic desensitization of NMDA receptors by calcineurin. Science 267: 1510-1512, 1995.
90. Tsai G and Coyle JT. Glutamatergic mechanisms in schizophrenia. Annu Rev Pharmacol Toxicol 42: 165-179, 2002.
91. Tsai G, Yang P, Chung L-C, Lange N, and Coyle JT. D-Serine added to antipsychotics for the treatment of schizophrenia. Biol Psychiatry 44: 1081-1089, 1998.
92. Tsai GE, Yang P, Chung LC, Tsai IC, Tsai CW, and Coyle JT. D-serine added to clozapine for the treatment of schizophrenia. Am J Psychiatry 156: 1822-1825, 1999.
93. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB, and Grayson DR. Functional and pharmacological differences between recombinant. N-methyl-D-aspartate receptors. J Neurophysiol 79: 555-566, 1998.
94. Vyklicky L Jr. Calcium-mediated modulation of N-methyl-D-aspartate (NMDA) responses in cultured rat hippocampal neurones. J Physiol 470: 575-600, 1993.
95. Vyklicky L Jr, Benveniste M, and Mayer ML. Modulation of N-methyl-D-aspartic acid receptor desensitization by glycine in mouse cultured hippocampal neurons. J Physiol 428: 313-331, 1990.
96. Weinberger DR and Berman KF. Prefrontal function in schizophrenia: confounds and controversies. Philos Trans R Soc Lond B Biol Sci 351: 1495-503, 1996.
97. Wood PL. The co-agonist concept: is the NMDA-associated glycine receptor saturated in vivo? Life Sci 57: 301-310, 1995.
98. Yang CR, Seamans JK, and Gorelova N. Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci 16: 1904-1921, 1996.
99. Yang CR, Seamans JK, and Gorelova N. Developing a neuronal model for the pathophysiology of schizophrenia based on the nature of electrophysiological actions of dopamine in the prefrontal cortex. Neuropsychopharmacology 21: 161-194, 1999.
100. Zafra F, Aragón C, and Gimenez C. Molecular biology of glycinergic neurotransmission. Mol Neurobiol 14: 117-142, 1997.
101. Zafra F, Aragón C, Oliveres L, Danbolt NC, Gimenez C, and Storm-Methisen J. Glycine transporters are differentially expressed among CNS cells. J Neurosci 15: 3952-3969, 1995.
102. Zilberter Y, Uteshev V, Sokolova S, and Khodorov B. Desensitization of N-methyl-D-aspartate receptors in neurons dissociated from adult rat hippocampus. Mol Pharmacol 40: 337-341, 1991.