D-Serine differently modulates NMDA receptor function in rat CA1 hippocampal pyramidal cells and interneurons

Journal of Physiology

Volumn 548, Issue 2, 2003, Pages 411-423

  Martina, Marzia ^a   Krasteniakov, Nicholas V ^a   Bergeron, Richard ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRO SERINE; GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RECEPTOR SUBUNIT; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL CELL; ARTICLE; BRAIN REGION; BRAIN SLICE; CELL KINETICS; CELL TYPE; CONTROLLED STUDY; DATA ANALYSIS; ELECTRIC POTENTIAL; HIPPOCAMPUS; INTERNEURON; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; RECORDING; REGULATORY MECHANISM; ANIMAL TISSUE; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL SLICE; STRATUM RADIATUM; WHOLE CELL PATCH CLAMP;

ANIMALS; AXONS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INTERNEURONS; KYNURENIC ACID; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLYCINE; RECEPTORS, N-METHYL-D-ASPARTATE; SERINE; TETRODOTOXIN;

EID: 0037731456     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.037127     Document Type: Article

References (80)

1. Amaral DG & Witter MP (1989). The three dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 32, 571-591.
2. + conductance by QX-314 in the rat hippocampus. Eur J Pharmacol 199, 259-262.
3. Ballard TM, Pauly-Evers M, Higgins GA, Ouagazzal A-M, Mutel V, Borroni E, Kemp JA, Bluethmann H & Kew JMC (2002). Severe impairment of NMDA receptor function in mice carrying targeted point mutations in the glycine binding site results in drug-resistant nonhabituating hyperactivity. J Neurosci 22, 6723-6723.
4. Benveniste M & Mayer ML (1991). Structure activity analysis of binding kinetics for NMDA receptor competitive antagonists: the influence of conformational restriction. Br J Pharmacol 104, 207-221.
5. Bergeron R, Meyer TM, Coyle JT & Greene RW (1998). Modulation of N-methyl-D-aspartate receptor function by glycine transport. Proc Natl Acad Sci U S A 95, 15 730-15 734.
6. Bliss TV & Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
7. Buller AM, Larson HC, Schneider BE, Beaton JA, Morrisett RA & Monaghan DT (1994). The molecular basis of NMDA receptor subtypes: native receptor diversity is predicted by subunit composition. J Neurosci 14, 5471-5484.
8. Carlsson M & Carlsson A (1990). Interaction between glutamatergic and monoaminergic system within the basal ganglia: Implication for schizophrenia and Parkinson's disease. Trends Neurosci 13, 272-276.
9. Chatterton JE, Awobuluyi M, Premkumar LS, Takahashi H, Talantova M, Shin Y, Cui J, Tu S, Sevarino KA, Nakanishi N, Tong G, Lipton SA & Zhang D (2002). Excitatory glycine receptors containing the NR3 family of NMDA receptor subunits. Nature 415, 793-798.
10. Ciabarra AM, Sullivan JM, Gahn LG, Petch G, Heinemann S & Saverino KA (1995). Cloning and characterization of chi-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15, 6498-6508.
11. 3H] dopamine release from rat striatal slices. Biochem Pharmacol 38, 4165-4168.
12. Czuczwar SJ & Meldrum B (1982). Protection against chemically induced seizures by 2-amino-7-phosphonoheptanoic acid. Eur J Pharmacol 83, 335-338.
13. Danysz W & Parsons AC (1998). Glycine and N-methyl-D-aspartate receptors: physiological significance and possible therapeutic applications. Pharmacol Rev 50, 597-664.
14. Das S, Sasaki YF, Rothe T, Premkumar LS, Takasu M, Crandall JE, Dikkes P, Conner DA, Rayudu PV, Cheung W, Chen HSV, Lipton SA & Nakanishi N (1998). Increased NMDA current and spine density in mice lacking the NMDA receptor subunit NR3A. Nature 393, 377-381.
15. Dingledine R, Borges K, Bowie D & Traynelis SF (1999). The glutamate receptor ion channels. Pharmacol Rev 51, 7-61.
16. Fletcher EJ & Lodge D (1988). 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.
17. Freund TF & Buzsáki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
18. Greene R (2001). Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus 11, 569-577.
19. Grunze HC, Rainnie DG, Hasselmo ME, Barkai E, Hearn EF, McCarley RW & Greene RW (1996). NMDA-dependent modulation of CA1 local circuit inhibition. J Neurosci 16, 2034-2043.
20. Hashimoto A, Kumashiro S, Nishikawa T, Oka T, Takahashi K, Mito T, Takashima S, Doi N, Mizutani Y & Yamazaki T (1993a). Embryonic development and postnatal changes in free D-aspartate and D-serine in the human prefrontal cortex. J Neurochem 61, 348-351.
21. Hashimoto A, Nishikawa T, Hayashi T, Fujii N, Harada K, Oka T & Takahashi K (1992). The presence of D-serine in rat brain. FEBS Lett 296, 33-36.
22. Hashimoto A, Nishikawa T, Oka T & Takahashi K (1993b). Endogenous D-serine in rat brain: N-methyl-D-aspartate receptor-related distribution and aging. J Neurochem 60, 783-786.
23. Hashimoto A & Oka T (1997). Free D-aspartate and D-serine in the mammalian brain and periphery. Prog Neurobiol 52, 325-353.
24. Hestrin S, Nicoll RA, Perkel DJ & Sah P (1990a). Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol 422, 203-225.
25. Hestrin S, Sah P & Nicoll RA (1990b). Mechanism generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 5, 247-253.
26. Hollmann M & Heinemann S (1994). Cloned glutamate receptors. Annu Rev Neurosci 17, 31-108.
27. Javitt DC & Zukin SR (1991). Recent advance in the phencyclidine model of schizophrenia. Am J Psychiatry 148, 1301-1308.
28. Johnson JW & Ascher P (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
29. Kemp JA, Foster AC, Leeson PD, Priestley T, Tridgett R, Iversen LL & Woodruff GN (1988). 7-Chlorokynurenic acid is a selective antagonist at the glycine modulatory site of N-methyl-D-aspartate receptor complex. Proc Natl Acad Sci U S A 85, 6547-6550.
30. Kemp JA & Leeson PD (1993). The glycine site of the NMDA receptor-five years on. Trends Pharmacol Sci 14, 20-25.
31. Kew JNC, Richards JG, Mutel V & Kemp JA (1998). Development 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.
32. Knowles WD & Schwartzkroin PA (1981). Local circuit synaptic interactions in hippocampal brain slices. J Neurosci 1, 318-322.
33. 2+ signals in spines of hippocampal neurons. J Neurosci 20, 1791-1799.
34. Kneisler TB & Dingledine R (1995a). Spontaneous and synaptic input from granule cells and perforant path to dentate basket cells in rat hippocampus. Hippocampus 5, 151-164.
35. Kneisler TB & Dingledine R (1995b). Synaptic input from CA3 pyramidal cells to dentate basket cells in rat hippocampus. J Physiol 487, 125-146.
36. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M & Mishina M (1992). Molecular diversity of NMDA receptor channel. Nature 358, 36-41.
37. Lacaille JC, Muller AL, Kunkel DD & Schwartzkroin PA (1987). Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 8, 1411-1424.
38. Laurie DJ & Seeburg PH (1994). Ligand affinities at recombinant N-methyl-D-aspartate receptors depend on subunit composition. Eur J Pharmacol 268, 335-345.
39. McBain CJ & Mayer ML (1994). N-methyl-D-aspartic acid receptor structure and function. Physiol Rev 74, 723-760.
40. MacDermott AB, Mayer ML, Westbrook GL, Smith SJ & Barker JL (1986). NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519-522.
41. Malenka RC & Nicoll RA (1999). Long-term potentiation: a decade of progress. Science 285, 1870-1874.
42. Matsui T, Sekiguchi M, Hashimoto A, Tomita U, Nishikawa T & Wada K (1995). Functional comparison of D-serine and glycine in rodents: the effect on cloned NMDA receptors and the extracellular concentration. J Neurochem 65, 454-458.
43. Mayer ML, Vyklicky L Jr & Clements J (1989). Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine. Nature 338, 425-427.
44. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K & Mishina M (1992). Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357, 70-74.
45. Meldrum B (1985). Possible therapeutic applications of antagonists of excitatory amino acid neurotransmitters. Clin Sci 68, 113-122.
46. Minota S, Miyazaki T, Wang MY, Read HL & Dun NJ (1989). Glycine potentiates NMDA responses in rat hippocampal CA1 neurons. Neurosci Lett 178, 139-143.
47. Misra C, Brickley SG, Wyllie DJA & Cull-Candy SG (2000). Slow deactivation kinetics of NMDA receptors containing NR1 and NR2D subunits in rat cerebellar Purkinje cells. J Physiol 525, 299-305.
48. Monyer H, Burnashev N, Laurie DJ, Sakmann B & Seeburg PH (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529-540.
49. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B & Seeburg PH (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221.
50. Morin F, Beaulieu C & Lacaille JC (1996). Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J Neurophysiol 76, 1-16.
51. Mothet JP, Parent AT, Wolosker H, Brady Ro JR, Linden DJ, Ferris CD, Rogawski MA & Snyder SH (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.
52. Nakanishi N (1992). Molecular diversity of glutamate receptors and implication for brain function. Science 258, 597-603.
53. Nakanishi N, Shneider NA & Axel R (1990). A family of glutamate receptor genes: evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5, 569-582.
54. Olney JW & Farber NB (1995). Glutamatergic receptor dysfunction and schizophrenia. Arch Gen Psychiat 52, 998-1007.
55. Parra P, Gulyás AI & Miles R (1998). How many subtypes if inhibitory cells in the hippocampus? Neuron 20, 983-993.
56. Perouansky M & Yaari Y (1993). Kinetic properties of NMDA receptor-mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. J Physiol 465, 223-244.
57. Priestley T & Kemp JA (1993). Agonist response kinetics of N-methyl-D-aspartate receptors in neurons cultured from rat cerebral cortex and cerebellum: evidence for receptor heterogeneity. Mol Pharmacol 44, 1252-1257.
58. Priestley T, Laughton P, Myers J, Le Bourdelles B, Kerby J & Whiting PJ (1995). Pharmacological properties of recombinant human N-methyl-D-aspartate receptors comprising NR1a/NR2A and NR1a/NR2B subunit assemblies expressed in permanently transfected mouse fibroblast cells. Mol Pharmacol 48, 841-848.
59. 3H] dopamine from rat striatal slices. Neurosci Lett 96, 323-328.
60. Riback CE & Peterson GM (1991). Intragranular mossy fiber in rats and gerbils from synapses with the somata and proximal dendrites of basket cells in the dentate gyrus. Hippocampus 1, 355-364.
61. Sah PJ, Hestrin S & Nicoll RA (1990). Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurones. J Physiol 430, 605-616.
62. Salt TE (1989). Modulation of NMDA receptor-mediated responses by glycine and D-serine in the rat thalamus in vivo. Brain Res 481, 403-406.
63. Schell MJ, Brady RO Jr, Molliver ME & Snyder SH (1997). D-Serine as a neuromodulator: regional and developmental localization in rat brain glia resemble NMDA receptors. J Neurosci 17, 1604-1615.
64. Schell MJ, Molliver ME & Snyder SH (1995). D-Serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci U S A 92, 3948-3952.
65. Schwartzkroin PA & Mathers LH (1978). Physiological and morphological identification of nonpyramidal hippocampal cell type. Brain Res 157, 1-10.
66. Seeburg PH (1996). The role of RNA editing in controlling glutamate receptor channel properties. J Neurochem 66, 1-5.
67. Semba J, Kito S & Toru M (1995). Characterisation of extracellular amino acids in striatum of freely moving rats by in vivo microdialysis. J Neural Transm Gen Sect 100, 39-52.
68. Smith KE, Borden LA, Hartig PR, Branchek T & Weinshank RL (1992). Cloning and expression of a glycine transporter reveal colocalization with NMDA receptors. Neuron 8, 927-935.
69. Sucher NJ, Akbarian S, Chi CL, Leclerc CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG & Lipton SA (1995). Developmental and regional expression pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15, 6509-6520.
70. Sucher NJ, Awobuluyi M, Choi YB & Lipton SA (1996). NMDA receptors: from genes to channels. Trends Pharmacol Sci 17, 348-355.
71. Supplisson S & Bergman C (1997). Control of NMDA receptor activation by a glycine transporter co-expressed in Xenopus oocytes. J Neurosci 17, 4580-4590.
72. Thiels E, Weisz DJ & Berger TW (1992). In vivo modulation of the N-methyl-D-aspartate receptor-dependent long-term potentiation by the glycine modulatory site. Neuroscience 46, 501-509.
73. Thomson AM, Walker VE & Flynn DM (1989). Glycine enhances NMDA-receptor mediated synaptic potentials in neocortical slices. Nature 338, 422-424.
74. Thomson JL, Bryan M, Bates T & Holmes GL (1988). Failure of kindling to alter the susceptibility to kainic acid. Brain Res 38, 149-151.
75. Vicini S, Wang JF, Li JH, Zhu WJ, Wang YH, Luo JH, Wolfe BB & Grayson DR (1998). Functional and pharmacological differences between recombinant N-methyl-D-aspartate receptors. J Neurophysiol 79, 555-566.
76. Westergren I, Nystrom B, Hamberger A, Nordborg C & Johansson B (1994). Concentration of amino acids in extracellular fluid after opening of the blood-brain barrier by intracarotid infusion of protamine sulfate. J Neurochem 62, 159-165.
77. Wilcox CS, Fitsimonds RM, Johnson B & Dichter MA (1996). Glycine regulation of synaptic NMDA receptors in hippocampal neurons. J Neurophysiol 76, 3415-3424.
78. Wood PL, Emmett MR, Rao TS, Mick S, Cler J & Iyengar S (1989). In vivo modulation of the N-methyl-D-aspartate receptor complex by D-serine: potentiation of ongoing neuronal activity as evidenced by increased cerebellar cyclic GMP. J Neurochem 53, 979-981.
79. Woodson W, Nitecka L & Ben-Ari Y (1989). Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J Comp Neurol 280, 354-271.
80. Yu W & Miller RF (1995). NBQX, an improved non-NMDA antagonist studied in retinal ganglion cells. Brain Res 692, 190-194.