Bergmann glial GlyT1 mediates glycine uptake and release in mouse cerebellar slices

Journal of Physiology

Volumn 560, Issue 3, 2004, Pages 721-736

  Huang, Hao ^a   Barakat, Latifa ^a   Wang, Doris ^a   Bordey, Angélique ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMINO ACID TRANSPORTER; CHLORIDE; GLYCINE; SARCOSINE; SODIUM ION; AMOXAPINE; GLYCINE TRANSPORTER; GLYCINE TRANSPORTER 1; GLYCINE TRANSPORTER 2; N [3 (4 FLUOROPHENYL) 3 (4 PHENYLPHENOXY)PROPYL]SARCOSINE; SODIUM;

AMINO ACID TRANSPORT; ANIMAL CELL; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CELL MEMBRANE POTENTIAL; CEREBELLUM; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GENE EXPRESSION; GLIA CELL; IMMUNOHISTOCHEMISTRY; ION CURRENT; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; REVIEW; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; ANIMAL TISSUE; ARTICLE; CELL LEVEL; CEREBELLAR SLICE; DEPOLARIZATION; GLIA; GRANULE CELL; INTRACELLULAR CHLORIDE; NEUROTRANSMITTER RELEASE; NEUROTRANSMITTER UPTAKE; OUTSIDE OUT PATCH CLAMP; WHOLE CELL PATCH CLAMP;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; CEREBELLUM; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; MICE; NEUROGLIA;

EID: 8844243233     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2004.067801     Document Type: Review

References (78)

1. Adams RH, Sato K, Shimada S, Tohyama M, Puschel AW & Betz H (1995). Gene structure and glial expression of the glycine transporter GlyT1 in embryonic and adult rodents. J Neurosci 15, 2524-2532.
2. Aragon MC, Gimenez C & Mayor F (1987). Stoichiometry of sodium- and chloride-coupled glycine transport in synaptic plasma membrane vesicles derived from rat brain. FEBS Lett 212, 87-90.
3. Atkinson BN, Bell SC, De Vivo M, Kowalski LR, Lechner SM, Ognyanov VI, Tham CS, Tsai C, Jia J, Ashton D & Klitenick MA (2001). ALX 5407: a potent, selective inhibitor of the hGlyT1 glycine transporter. Mol Pharmacol 60, 1414-1420.
4. Attwell D, Barbour B & Szatkowski M (1993). Nonvesicular release of neurotransmitter. Neuron 11, 401-407.
5. Aubrey KR & Vandenberg RJ (2001). N[3-(4′-fluorophenyl)-3-(4′-phenylphenoxy) propyl]sarcosine (NFPS) is a selective persistent inhibitor of glycine transport. Br J Pharmacol 134, 1429-1436.
6. Barakat L & Bordey A (2002). GAT-1 and reversible GABA transport in Bergmann glia in slices. J Neurophysiol 88, 1407-1419.
7. Barakat L, Wang D & Bordey A (2002). Carrier-mediated uptake and release of taurine from Bergmann glia in rat cerebellar slices. J Physiol 541, 753-767.
8. Baranano DE, Ferris CD & Snyder SH (2001). Atypical neural messengers. Trends Neurosci 24, 99-106.
9. Barbour B, Brew H & Attwell D (1990). Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander retina. J Physiol 436, 169-194.
10. Barker GA & Ellory JC (1990). The identification of neutral amino acid transport systems. Exp Physiol 75, 3-26.
11. Bekar LK & Walz W (2002). Intracellular chloride modulates A-type potassium currents in astrocytes. Glia 39, 207-216.
12. Berger SJ, Carter JC & Lowry OH (1977). The distribution of glycine, GABA, glutamate and aspartate in rabbit spinal cord, cerebellum and hippocampus. J Neurochem 28, 149-158.
13. 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, 15730-15734.
14. Borden LA (1996). GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29, 335-356.
15. Bordey A & Sontheimer H (1997). Postnatal development of ionic currents in rat hippocampal astrocytes in situ. J Neurophysiol 78, 461-477.
16. Bordey A & Sontheimer H (2000). Ion channel expression by astrocytes in situ: comparison of different CNS regions. Glia 30 27-38.
17. Bormann J, Hamill OP & Sakmann B (1987). Mechanism of anion permeation through channels gated by glycine and gamma-aminobutyric acid in mouse cultured spinal neurones. J Physiol 385, 243-286.
18. Casado M, Isope P & Ascher P (2002). Involvement of presynaptic N-methyl-D-aspartate receptors in cerebellar long-term depression. Neuron 33, 123-130.
19. Caulfield WL, Collie IT, Dickins RS, Epemolu O, McGuire R, Hill DR, McVey G, Morphy JR, Rankovic Z & Sundaram H (2001). The first potent and selective inhibitors of the glycine transporter type 2. J Medicalchem 44, 2679-2682.
20. Chen L, Muhlhauser M & Yang CR (2003). Glycine tranporter-1 blockade potentiates NMDA-mediated responses in rat prefrontal cortical neurons in vitro and in vivo. J Neurophysiol 89, 691-703.
21. Christensen HN (1984). Organic ion transport during seven decades. The amino acids. Biochim Biophys Acta 779, 255-269.
22. Dalkara T, Tan T & Onur R (1990). Glycine, alanine and serine potentiate glutamate neurotoxicity in cerebral ischemia via NMDA receptors. Eur J Pharmacol 183, 476.
23. Danysz W & Parsons AC (1998). Glycine and N-methyl-D-aspartate receptors: physiological significance and possible therapeutic applications. Pharmacol Rev 50, 597-664.
24. de Blas AL (1984). Monoclonal antibodies to specific astroglial and neuronal antigens reveal the cytoarchitecture of the Bergmann glia fibers in the cerebellum. J Neurosci 4, 265-273.
25. Diamond JS & Jahr CE (2000). Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. J Neurophysiol 83, 2835-2843.
26. Dumoulin A, Triller A & Dieudonne S (2001). IPSC kinetics at identified GABAergic and mixed GABAergic and glycinergic synapses onto cerebellar Golgi cells. J Neurosci 21, 6045-6057.
27. Fedele E, Bisaglia M & Raiteri M (1997). D-serine modulates the NMDA receptor/nitric oxide/cGMP pathway in the rat cerebellum during in vivo microdialysis. Naunyn Schmiedebergs Arch Pharmacol 355 43-47.
28. Gadea A, Lopez E & Lopez-Colome AM (1999). Characterization of glycine transport in cultured Muller glial cells from the retina. Glia 26, 273-279.
29. Gadea A & Lopez-Colome AM (2001). Glial transporters for glutamate, glycine, and GABA III. Glycine transporters. J Neurosci Res 64, 218-222.
30. Glitsch M & Marty A (1999). Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19, 511-519.
31. Gomeza J, Hulsmann S, Ohno K, Eulenburg V, Szoke K, Richter D & Betz H (2003a). Inactivation of the glycine transporter 1 gene discloses vital role of glial glycine uptake in glycinergic inhibition. Neuron 40, 785-796.
32. Gomeza J, Ohno K, Hulsmann S, Armsen W, Eulenburg V, Richter DW, Laube B & Betz H (2003b). Deletion of the mouse glycine transporter 2 results in a hyperekplexia phenotype and postnatal lethality. Neuron 40, 797-806.
33. Guastella J, Brecha N, Weigmann C, Lester HA & Davidson N (1992). Cloning, expression, and localization of a rat brain high-affinity glycine transporter. Proc Natl Acad Sci U S A 89 7189-7193.
34. Holopainen I & Kontro P (1989). Uptake and release of glycine in cerebellar granule cells and astrocytes in primary culture: potassium-stimulated release from granule cells is calcium-dependent. J Neurosci Res 24, 374-383.
35. Huang H & Bordey A (2004). Glial glutamate transporters limit spillover activation of presynaptic NMDA receptors and influence synaptic inhibition of Purkinje neurons. J Neurosci 24, 5659-5669.
36. Johnson JW & Ascher P (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
37. Kaneda M, Farrant M & Cull-Candy SG (1995). Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol 485, 419-435.
38. Kinney GG, Sur C, Burno M, Mallorga PJ, Williams JB, Figueroa DJ, Wittmann M, Lemaire W & Conn PJ (2003). The glycine transporter type 1 inhibitor N-[3-(4′-fluorophenyl)-3-(4′-phenylphenoxy) propyl]sarcosine potentiates NMDA receptor-mediated responses in vivo and produces an antipsychotic profile in rodent behavior. J Neurosci 23, 7586-7591.
39. Kleckner NW & Dingledine R (1988). Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241, 835-837.
40. Kyrozis A & Reichling DB (1995). Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Meth 57, 27-35.
41. Liu QR, Lopez-Corcuera B, Mandiyan S, Nelson H & Nelson N (1993). Cloning and expression of a spinal cord- and brain-specific glycine transporter with novel structural features. J Biol Chem 268, 22802-22808.
42. Liu QR, Lopez-Corcuera B, Nelson H, Mandiyan S & Nelson N (1992). Cloning and expression of a cDNA encoding the transporter of taurine and beta-alanine in mouse brain. Proc Natl Acad Sci U S A 89, 12145-12149.
43. Llano I, Marty A, Armstrong CM & Konnerth A (1991). Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol 434, 183-213.
44. Lopez-Corcuera B, Liu QR, Mandiyan S, Nelson H & Nelson N (1992). Expression of a mouse brain cDNA encoding novel gamma- aminobutyric acid transporter. J Biol Chem 267, 17491-17493.
45. Lopez-Corcuera B, Martinez-Maza R, Nunez E, Roux M, Supplisson S & Aragon C (1998). Differential properties of two stably expressed brain-specific glycine transporters. J Neurochem 71 2211-2219.
46. Mallorga PJ, Williams JB, Jacobson M, Marques R, Chaudhary A, Conn PJ, Pettibone DJ & Sur C (2003). Pharmacology and expression analysis of glycine transporter GlyT1 with [3H]-(N-[3-(4′-fluorophenyl)-3-(4′phenylphenoxy) propyl]) sarcosine. Neuropharmacology 45, 585-593.
47. Matskevitch I, Wagner CA, Stegen C, Broer S, Noll B, Risler T, Kwon HM, Handler JS, Waldegger S, Busch AE & Lang F (1999). Functional characterization of the Betaine/gamma-aminobutyric acid transporter BGT-1 expressed in Xenopus oocytes. J Biol Chem 274, 16709-16716.
48. Mayer ML, Vyklicky L Jr & Clements J (1989). Regulation of NMDA receptor desensitization in mouse hippocampal neurons by glycine. Nature 338, 425-427.
49. Miranda-Contreras L, Benitez-Diaz PR, Mendoza-Briceno RV, Delgado-Saez MC & Palacios-Pru EL (1999). Levels of amino acid neurotransmitters during mouse cerebellar neurogenesis and in histotypic cerebellar cultures. Dev Neurosci 21, 147-158.
50. Morara S, Brecha NC, Marcotti W, Provini L & Rosina A (1996). Neuronal and glial localization of the GABA transporter GAT-1 in the cerebellar cortex. Neuroreport 7, 2993-2996.
51. Morrow JA, Collie IT, Dunbar DR, Walker GB, Shahid M & Hill DR (1998). Molecular cloning and functional expression of the human glycine transporter GlyT2 and chromosomal localisation of the gene in the human genome. FEBS Lett 439, 334-340.
52. A receptor expression in Bergmann glial cells. J Neurosci 14, 2503-2514.
53. Myers VB & Haydon DA (1972). Ion transfer across lipid membranes in the presence of gramicidin A. II. The ion selectivity. Biochim Biophys Acta 274, 313-322.
54. Nong Y, Huang YQ, Ju W, Kalia LV, Ahmadian G, Wang YT & Salter MW (2003). Glycine binding primes NMDA receptor internalization. Nature 422, 302-307.
55. Nunez E, Lopez-Corcuera B, Vazquez J, Gimenez C & Aragon C (2000). Differential effects of the tricyclic antidepressant amoxapine on glycine uptake mediated by the recombinant GLYT1 and GLYT2 glycine transporters. Br J Pharmacol 129, 200-206.
56. Palacin M, Estevez R, Bertran J & Zorzano A (1998). Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev 78, 969-1054.
57. Palay SL & Chan-Palay V (1974). Cerebellar Cortex, Cytology and Organization, pp. 236. Springer-Verlag, New York.
58. Parsons CG, Danysz W, Hesselink M, Hartmann S, Lorenz B, Wollenburg C & Quack G (1998). Modulation of NMDA receptors by glycine - introduction to some basic aspects and recent developments. Amino Acids 14, 207-216.
59. Rao TS, Cler JA, Emmett MR, Mick SJ, Iyengar S & Wood PL (1990). Glycine, glycinamide and D-serine act as positive modulators of signal transduction at the N-methyl-D-aspartate (NMDA) receptor in vivo: differential effects on mouse cerebellar cyclic guanosine monophosphate levels. Neuropharmacology 29, 1075-1080.
60. Reichenbach A, Siegel A, Rickmann M, Wolff JR, Noone D & Robinson SR (1995). Distribution of Bergmann glial somata and processes: implications for function. J Hirnforsch 36, 509-517.
61. Rose CR & Ransom BR (1996a). Intracellular sodium homeostasis in rat hippocampal astrocytes. J Physiol 491, 291-305.
62. + changes induced by glutamate, kainate, and D-aspartate in rat hippocampal astrocytes. J Neurosci 16, 5393-5404.
63. Rosenmund C, Legendre P & Westbrook GL (1992). Expression of NMDA channels on cerebellar Purkinje cells acutely dissociated from newborn rats. J Neurophysiol 68, 1901-1905.
64. Roux MJ & Supplisson S (2000). Neuronal and glial glycine transporters have different stoichiometries. Neuron 25, 373-383.
65. Sakata K, Sato K, Schloss P, Betz H, Shimada S & Tohyama M (1997). Characterization of glycine release mediated by glycine transporter 1 stably expressed in HEK-293 cells. Brain Res Mol Brain Res 49, 89-94.
66. Saransaari P & Oja SS (1994). Glycine release from hippocampal slices in developing and ageing mice: modulation by glutamatergic receptors. Mech Ageing Dev 76, 113-124.
67. Saransaari P & Oja SS (2001). Characteristics of hippocampal glycine release in cell-damaging conditions in the adult and developing mouse. Neurochem Res 26, 845-852.
68. Schell MJ, Brady RO Jr, Molliver ME & Snyder SH (1997). D-serine as a neuromodulator: regional and developmental localizations in rat brain glia resemble NMDA receptors. J Neurosci 17, 1604-1615.
69. 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.
70. A receptors. Science 269 977-981.
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. Swan M, Najlerahim A, Watson RE & Bennett JP (1994). Distribution of mRNA for the GABA transporter GAT-1 in the rat brain: evidence that GABA uptake is not limited to presynaptic neurons. J Anat 185, 315-323.
73. Thomson AM, Walker VE & Flynn DM (1989). Glycine enhances NMDA-receptor mediated synaptic potentials in neocortical slices. Nature 338, 422-424.
74. White WF, Brown KL & Frank DM (1989). Glycine binding to rat cortex and spinal cord: binding characteristics and pharmacology reveal distinct populations of sites. J Neurochem 53, 503-512.
75. Wood PL (1995). The co-agonist concept: is the NMDA-associated glycine receptor saturated in vivo? Life Sci 57, 301-310.
76. 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.
77. Zafra F, Aragon C, Olivares L, Danbolt NC, Gimenez C & Storm-Mathisen J (1995). Glycine transporters are differentially expressed among CNS cells. J Neurosci 15, 3952-3969.
78. Zafra F & Gimenez C (1989). Characteristics and adaptive regulation of glycine transport in cultured glial cells. Biochem J 258, 403-408.