The role of glutamate transporters in synaptic transmission

Structural And Functional Organization Of The Synapse

Volumn , Issue , 2008, Pages 23-61

  Bergles, Dwight E ^a   Edwards, Robert H ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84862618303     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-77232-5_2     Document Type: Chapter

References (227)

1. Accardi A and Miller C. Secondary active transport mediated by a prokaryotic homologue of ClC Cl-channels. Nature 427: 803-807, 2004.
2. Ahnert-Hilger G, Nurnberg B, Exner T, Schafer T, and Jahn R. The heterotrimeric G protein G02 regulates catecholamine uptake by secretory vesicles. EMBO J 17: 406-413, 1998.
3. Aihara Y, Mashima H, Onda H, Hisano S, Kasuya H, Hori T, Yamada S, Tomura H, Yamada Y, Inoue I, Kojima I, and Takeda J. Molecular cloning of a novel brain-type Na(+)-dependent inorganic phosphate cotransporter. J Neurochem 74: 2622-2625, 2000.
4. Albuquerque EX, Barnard EA, Porter CW, and Warnick JE. The density of acetylcholine receptors and their sensitivity in the postsynaptic membrane of muscle endplates. Proc Natl Acad Sci USA 71: 2818-2822, 1974.
5. Amara SG and Kuhar MJ. Neurotransmitter transporters: recent progress. Annu Rev Neurosci 16: 73-93, 1993.
6. Armano S, Coco S, Bacci A, Pravettoni E, Schenk U, Verderio C, Varoqui H, Erickson JD, and Matteoli M. Localization and functional relevance of system a neutral amino acid transporters in cultured hippocampal neurons. J Biol Chem 277: 10467-10473, 2002.
7. Arnth-Jensen N, Jabaudon D, and Scanziani M. Cooperation between independent hippocampal synapses is controlled by glutamate uptake. Nat Neurosci 5: 325-331, 2002.
8. Arriza JL, Eliasof S, Kavanaugh MP, and Amara SG. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc Natl Acad Sci USA 94: 4155-4160, 1997.
9. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, and Amara SG. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14: 5559-5569, 1994.
10. Auger C and Attwell D. Fast removal of synaptic glutamate by postsynaptic transporters. Neuron 28: 547-558, 2000.
11. Bacci A, Sancini G, Verderio C, Armano S, Pravettoni E, Fesce R, Franceschetti S, and Matteoli M. Block of glutamate-glutamine cycle between astrocytes and neurons inhibits epileptiform activity in hippocampus. J Neurophysiol 88: 2302-2310, 2002.
12. Bankston LA and Guidotti G. Characterization of ATP transport into chromaffin granule ghosts. Synergy of ATP and serotonin accumulation in chromaffin granule ghosts. J Biol Chem 271: 17132-17138, 1996.
13. Barasch J, Gershon MD, Nunez EA, Tamir H, and al-Awqati Q. Thyrotropin induces the acidification of the secretory granules of parafollicular cells by increasing the chloride conductance of the granular membrane. J Cell Biol 107: 2137-2147, 1988.
14. Barberis A, Petrini EM, and Cherubini E. Presynaptic source of quantal size variability at GABAergic synapses in rat hippocampal neurons in culture. Eur J Neurosci 20: 1803-1810, 2004.
15. Barbour B, Brew H, and Attwell D. Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystoma) retina. J Physiol (Lond) 436: 169-193, 1991.
16. Barbour B and Hausser M. Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377-384, 1997.
17. Bekkers JM, Richerson GB, and Stevens CF. Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. Proc Natl Acad Sci USA 87: 5359-5362, 1990a.
18. Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, and Edwards RH. The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18: 8648-8659, 1998.
19. Bellocchio EE, Reimer RJ, Fremeau RTJ, and Edwards RH. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289: 957-960, 2000.
20. Bergles DE, Dzubay JA, and Jahr CE. Glutamate transporter currents in bergmann glial cells follow the time course of extrasynaptic glutamate. Proc Natl Acad Sci USA 94: 14821-14825, 1997.
21. Bergles DE and Jahr CE. Glial contribution to glutamate uptake at Schaffer collateralcommissural synapses in the hippocampus. J Neurosci 18: 7709-7716, 1998.
22. Bergles DE and Jahr CE. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19: 1297-1308, 1997.
23. Bergles DE, Tzingounis AV, and Jahr CE. Comparison of coupled and uncoupled currents during glutamate uptake by GLT-1 transporters. J Neurosci 22: 10153-10162, 2002.
24. Bole DG, Hirata K, and Ueda T. Prolonged depolarization of rat cerebral synaptosomes leads to an increase in vesicular glutamate content. Neurosci Lett 322: 17-20, 2002.
25. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT, Jr., Edwards RH, Storm-Mathisen J, and Chaudhry FA. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480: 264-280, 2004.
26. Brasnjo G and Otis TS. Isolation of glutamate transport-coupled charge flux and estimation of glutamate uptake at the climbing fiber-Purkinje cell synapse. Proc Natl Acad Sci USA 101: 6273-6278, 2004.
27. Brasnjo G and Otis TS. Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31: 607-616, 2001.
28. Bröer S, Schuster A, Wagner CA, Bröer A, Forster I, Biber J, Murer H, Werner A, Lang F, and Busch AE. Chloride conductance and Pi transport are separate functions induced by the expression of NaPi-1 in Xenopus oocytes. J Memb Biol 164: 71-77, 1998.
29. Brunk I, Blex C, Rachakonda S, Holtje M, Winter S, Pahner I, Walther DJ, and Ahnert-Hilger G. The first luminal domain of vesicular monoamine transporters mediates Gprotein-dependent regulation of transmitter uptake. J Biol Chem 281: 33373-33385, 2006.
30. Bruns D, Riedel D, Klingauf J, and Jahn R. Quantal release of serotonin. Neuron 28: 205-220, 2000.
31. Busch AE, Schuster A, Waldegger S, Wagner CA, Zempel G, Broer S, Biber J, Murer H, and Lang F. Expression of a renal type I sodium/phosphate transporter (NaPi-1) induces a conductance in Xenopus oocytes permeable for organic and inorganic anions. Proc Natl Acad Sci USA 93: 5347-5351, 1996.
32. Cabeza R and Collier B. Acetylcholine mobilization in a sympathetic ganglion in the presence and absence of 2-(4-phenylpiperidino)cyclohexanol (AH5183). J Neurochem 50: 112-121, 1988.
33. Carlson MD, Kish PE, and Ueda T. Characterization of the solubilized and reconstituted ATP-dependent vesicular glutamate uptake system. J Biol Chem 264: 7369-7376, 1989a.
34. Carter AG and Regehr WG. Prolonged synaptic currents and glutamate spillover at the parallel fiber to stellate cell synapse. J Neurosci 20: 4423-4434, 2000.
35. Chaudhry FA, Reimer RJ, and Edwards RH. The glutamine commute: take the N line and transfer to the A. J Cell Biol 157: 349-355, 2002b.
36. Chen S and Diamond JS. Synaptically released glutamate activates extrasynaptic NMDA receptors on cells in the ganglion cell layer of rat retina. J Neurosci 22: 2165-2173, 2002.
37. Chen W, Mahadomrongkul V, Berger UV, Bassan M, DeSilva T, Tanaka K, Irwin N, Aoki C, and Rosenberg PA. The glutamate transporter GLT1a is expressed in excitatory axon terminals of mature hippocampal neurons. J Neurosci 24: 1136-1148, 2004.
38. Clark BA and Cull-Candy SG. Activity-dependent recruitment of extrasynaptic NMDA receptor activation at an AMPA receptor-only synapse. J Neurosci 22: 4428-4436, 2002.
39. Clements JD. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci 19: 163-171, 1996.
40. Colliver TL, Pyott SJ, Achalabun M, and Ewing AG. VMAT-Mediated changes in quantal size and vesicular volume. J Neurosci 20: 5276-5282, 2000.
41. Conti F, DeBiasi S, Minelli A, Rothstein JD, and Melone M. EAAC1, a high-affinity glutamate tranporter, is localized to astrocytes and gabaergic neurons besides pyramidal cells in the rat cerebral cortex. Cereb Cortex 8: 108-116, 1998.
42. Conti F and Minelli A. Glutamate immuoreactivity in rat cerebral cortex is reversibly abolished by 6-diazo-5-oxo-L-norleucine. J Histochem Cytochem 42: 717-726, 1994.
43. Croft BG, Fortin GD, Corera AT, Edwards RH, Beaudet A, Trudeau LE, and Fon EA. Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol Biol Cell 16: 306-315, 2005.
44. Crowder KM, Gunther JM, Jones TA, Hale BD, Zhang HZ, Peterson MR, Scheller RH, Chavkin C, and Bajjalieh SM. Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A). Proc Natl Acad Sci USA 96: 15268-15273, 1999.
45. Curthoys NP and Watford M. Regulation of glutaminase activity and glutamine metabolism. Ann Rev Nutr 15: 133-159, 1995.
46. Danbolt NC. Glutamate uptake. Prog Neurobiol 65: 1-105, 2001.
47. Daniels RW, Collins CA, Chen K, Gelfand MV, Featherstone DE, and Diantonio A. A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron 49: 11-16, 2006.
48. Daniels RW, Collins CA, Gelfand MV, Dant J, Brooks ES, Krantz DE, and DiAntonio A. Increased expression of the Drosophila vesicular glutamate transporter leads to excess glutamate release and a compensatory decrease in quantal content. J Neurosci 24: 10466-10474, 2004.
49. Dehnes Y, Chaudhry FA, Ullensvang K, Lehre KP, Storm-Mathisen J, and Danbolt NC. The glutamate transporter EAAT4 in rat cerebellar Purkinje cells: a glutamate-gated chloride channel concentrated near the synapse in parts of the dendritic membrane facing astroglia. J Neurosci 18: 3606-3619, 1998.
50. Diamond JS. Deriving the glutamate clearance time course from transporter currents in CA1 hippocampal astrocytes: transmitter uptake gets faster during development. J Neurosci 25: 2906-2916, 2005.
51. Diamond JS and Jahr CE. Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation. J Neurophysiol 83: 2835-2843, 2000.
52. Diamond JS and Jahr CE. Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci 17: 4672-4687, 1997.
53. Dickman DK, Horne JA, Meinertzhagen IA, and Schwarz TL. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking synaptojanin and endophilin. Cell 123: 521-533, 2005.
54. Doherty P, Hawgood BJ, and Smith IC. Changes in miniature end-plate potentials after brief nervous stimulation at the frog neuromuscular junction. J Physiol 356: 349-358, 1984.
55. Drory O and Nelson N. The emerging structure of vacuolar ATPases. Physiology (Bethesda) 21: 317-325, 2006.
56. Dunant Y and Israel M. Neurotransmitter release at rapid synapses. Biochimie 82: 289-302, 2000.
57. Elhamdani A, Palfrey HC, and Artalejo CR. Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31: 819-830, 2001.
58. Fairman WA, Vandenberg RJ, Arriza JL, Kavanaugh MP, and Amara SG. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375: 599-603, 1995.
59. Fernandez-Peruchena C, Navas S, Montes MA, and Alvarez de Toledo G. Fusion pore regulation of transmitter release. Brain Res Brain Res Rev 49: 406-415, 2005.
60. Fon EA, Pothos EN, Sun B-C, Killeen N, Sulzer D, and Edwards RH. Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action. Neuron 19: 1271-1283, 1997.
61. Forgac M. Structure, mechanism and regulation of the clathrin-coated vesicle and yeast vacuolar H(+)-ATPases. J Exp Biol 203 Pt 1: 71-80, 2000.
62. Forti L, Bossi M, Bergamaschi A, Villa A, and Malgaroli A. Loose-patch recordings of single quanta at individual hippocampal synapses. Nature 388: 874-878, 1997.
63. Fremeau RT, Jr., Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, and Edwards RH. The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99: 14488-14493, 2002.
64. Fremeau RT, Jr., Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, and Edwards RH. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304: 1815-1819, 2004.
65. Fremeau RT, Jr., Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, and Edwards RH. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260, 2001.
66. Frerking M and Wilson M. Effects of variance in mini amplitude on stimulus-evoked release: a comparison of two models. Biophys J 70: 2078-2091, 1996.
67. Furness DN and Lehre KP. Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur J Neurosci 9: 1961-1969, 1997.
68. Genoud C, Quairiaux C, Steiner P, Hirling H, Welker E, and Knott GW. Plasticity of astrocytic coverage and glutamate transporter expression in adult mouse cortex. PLoS Biol 4: e343, 2006.
69. Gillespie DC, Kim G, and Kandler K. Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci 8: 332-338, 2005.
70. Ginsberg SD, Rothstein JD, Price DL, and Martin LJ. Fimbria-fornix transections selectively down-regulate subtypes of glutamate transporter and glutamate receptor proteins in septum and hippocampus. J Neurochem 67: 1208-1216, 1996.
71. Giompres PE, Zimmermann H, and Whittaker VP. Changes in the biochemical and biophysical parameters of cholinergic synaptic vesicles on transmitter release and during a subsequent period of rest. Neuroscience 6: 775-785, 1981.
72. Glowatzki E, Cheng N, Hiel H, Yi E, Tanaka K, Ellis-Davies GC, Rothstein JD, and Bergles DE. The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea. J Neurosci 26: 7659-7664, 2006.
73. Gong LW, Hafez I, Alvarez de Toledo G, and Lindau M. Secretory vesicles membrane area is regulated in tandem with quantal size in chromaffin cells. J Neurosci 23: 7917-7921, 2003.
74. Grabner CP, Price SD, Lysakowski A, Cahill AL, and Fox AP. Regulation of large dense-core vesicle volume and neurotransmitter content mediated by adaptor protein 3. Proc Natl Acad Sci USA 103: 10035-10040, 2006.
75. Grabner CP, Price SD, Lysakowski A, and Fox AP. Mouse chromaffin cells have two populations of dense core vesicles. J Neurophysiol 94: 2093-2104, 2005.
76. Gracz LM, Wang W-C, and Parsons SM. Cholinergic synaptic vesicle heterogeneity: evidence for regulation of acetylcholine transport. Biochem 27: 5268-5274, 1988.
77. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, and El Mestikawy S. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22: 5442-5451, 2002.
78. Hajos N, Nusser Z, Rancz EA, Freund TF, and Mody I. Cell type-and synapse-specific variability in synaptic GABAA receptor occupancy. Eur J Neurosci 12: 810-818, 2000.
79. Hakuba N, Koga K, Gyo K, Usami S-i, and Tanaka K. Exacerbation of Noise-Induced Hearing Loss in Mice Lacking the Glutamate Transporter GLAST. J Neurosci 20: 8750-8753, 2000.
80. Hamberger A, Chiang GH, Sandoval E, and Cotman CW. Glutamate as a CNS transmitter. II. Regulation of synthesis in the releasable pool. Brain Res 168: 531-541, 1979b.
81. Harata NC, Aravanis AM, and Tsien RW. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J Neurochem 97: 1546-1570, 2006.
82. Harkany T, Holmgren C, Hartig W, Qureshi T, Chaudhry FA, Storm-Mathisen J, Dobszay MB, Berghuis P, Schulte G, Sousa KM, Fremeau RT, Jr., Edwards RH, Mackie K, Ernfors P, and Zilberter Y. Endocannabinoid-independent retrograde signaling at inhibitory synapses in layer 2/3 of neocortex: involvement of vesicular glutamate transporter 3. J Neurosci 24: 4978-4988, 2004.
83. Hartinger J and Jahn R. An anion binding site that regulates the glutamate transporter of synaptic vesicles. J Biol Chem 268: 23122-23127, 1993.
84. Hartman KN, Pal SK, Burrone J, and Murthy VN. Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci 9: 642-649, 2006.
85. Hasegawa J, Obara T, Tanaka K, and Tachibana M. High-density presynaptic transporters are required for glutamate removal from the first visual synapse. Neuron 50: 63-74, 2006.
86. Hausser M and Roth A. Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol (Lond) 501: 77-95, 1997.
87. He Y, Janssen WG, Rothstein JD, and Morrison JH. Differential synaptic localization of the glutamate transporter EAAC1 and glutamate receptor subunit GluR2 in the rat hippocampus. J Comp Neurol 418: 255-269, 2000.
88. Hell JW, Maycox PR, and Jahn R. Energy dependence and functional reconstitution of the gamma-aminobutyric acid carrier from synaptic vesicles. J Biol Chem 265: 2111-2117, 1990.
89. Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, and El Mestikaway S. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21: RC181, 2001.
90. 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.
91. Hiesinger PR, Fayyazuddin A, Mehta SQ, Rosenmund T, Schulze KL, Zhai RG, Verstreken P, Cao Y, Zhou Y, Kunz J, and Bellen HJ. The v-ATPase V0 subunit a1 is required for a late step in synaptic vesicle exocytosis in Drosophila. Cell 121: 607-620, 2005.
92. Holmseth S, Dehnes Y, Bjornsen LP, Boulland JL, Furness DN, Bergles D, and Danbolt NC. Specificity of antibodies: unexpected cross-reactivity of antibodies directed against the excitatory amino acid transporter 3 (EAAT3). Neuroscience 136: 649-660, 2005.
93. Höltje M, von Jagow B, Pahner I, Lautenschlager M, Hörtnagl H, Nürnberg B, Jahn R, and Ahnert-Hilger G. The neuronal monoamine transporter VMAT2 is regulated by the trimeric GTPase Go(2). J Neurosci 20: 2131-2141, 2000.
94. Huang YH, Dykes-Hoberg M, Tanaka K, Rothstein JD, and Bergles DE. Climbing fiber activation of EAAT4 transporters and kainate receptors in cerebellar Purkinje cells. J Neurosci 24: 103-111, 2004.
95. Huang YH, Sinha SR, Tanaka K, Rothstein JD, and Bergles DE. Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J Neurosci 24: 4551-4559, 2004.
96. Huggett J, Vaughan-Thomas A, and Mason D. The open reading frame of the Na(+)-dependent glutamate transporter GLAST-1 is expressed in bone and a splice variant of this molecule is expressed in bone and brain. FEBS Lett 485: 13-18, 2000.
97. Isaacson JS and Nicoll RA. The uptake inhibitor L-trans-PDC enhances responses to glutamate but fails to alter the kinetics of excitatory synaptic currents in the hippocampus. J Neurophysiol 70: 2187-2191, 1993.
98. Ishikawa T, Sahara Y, and Takahashi T. A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34: 613-621, 2002.
99. Jabaudon D, Shimamoto K, Yasuda-Kamatani Y, Scanziani M, Gahwiler BH, and Gerber U. Inhibition of uptake unmasks rapid extracellular turnover of glutamate of nonvesicular origin. Proc Natl Acad Sci USA 96: 8733-8738, 1999.
100. Janz R, Goda Y, Geppert M, Missler M, and Südhof TC. SV2A and SV2B function as redundant Ca2+ regulators in neurotransmitter release. Neuron 24: 1003-1016, 1999.
101. Jentsch TJ, Poet M, Fuhrmann JC, and Zdebik AA. Physiological functions of CLC Clchannels gleaned from human genetic disease and mouse models. Annu Rev Physiol 67: 779-807, 2005.
102. Johnson RG. Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiol Rev 68: 232-307, 1988.
103. Juge N, Yoshida Y, Yatsushiro S, Omote H, and Moriyama Y. Vesicular glutamate transporter contains two independent transport machineries. J Biol Chem 281: 39499-39506, 2006.
104. Kam K and Nicoll R. Excitatory synaptic transmission persists independently of the glutamate-glutamine cycle. J Neurosci 27: 9192-9200, 2007.
105. Kane PM. Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J Biol Chem 270: 17025-17032, 1995.
106. Karunanithi S, Marin L, Wong K, and Atwood HL. Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22: 10267-10276, 2002.
107. Katagiri H, Tanaka K, and Manabe T. Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 14: 547-553, 2001.
108. Katz B. Quantal mechanism of neural transmitter release. Science 173: 123-126, 1971.
109. Kawasaki-Nishi S, Bowers K, Nishi T, Forgac M, and Stevens TH. The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J Biol Chem 276: 47411-47420, 2001.
110. Kish PE, Fischer-Bovenkerk C, and Ueda T. Active transport of gamma-aminobutyric acid and glycine into synaptic vesicles. Proc Natl Acad Sci USA 86: 3877-3881, 1989.
111. Kozminski KD, Gutman DA, Davila V, Sulzer D, and Ewing AG. Voltammetric and pharmacological characterization of dopamine release from single exocytotic events at rat pheochromocytoma (PC12) cells. Anal Chem 70: 3123-3130, 1998.
112. Kvamme E, Torgner IA, and Roberg B. Kinetics and localization of brain phosphate activated glutaminase. J Neurosci Res 66: 951-958, 2001.
113. Laake JH, Slyngstad TA, Haug FM, and Ottersen OP. Glutamine from glial cells is essential for the maintenance of the nerve terminal pool of glutamate: immunogold evidence from hippocampal slice cultures. J Neurochem 65: 871-881, 1995.
114. Lehre KP and Danbolt NC. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18: 8751-8757, 1998.
115. Lehre KP, Levy LM, Ottersen OP, Storm-Mathisen J, and Danbolt NC. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J Neurosci 15: 1835-1853, 1995.
116. Lehre KP and Rusakov DA. Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys J 83: 125-134, 2002.
117. Levy LM, Warr O, and Attwell D. Stoichiometry of the glial glutamate transporter GLT-1 expressed inducibly in a Chinese hamster ovary cell line selected for low endogenous Na+-dependent glutamate uptake. J Neurosci 18: 9620-9628, 1998.
118. Liang SL, Carlson GC, and Coulter DA. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci 26: 8537-8548, 2006.
119. Liu G, Choi S, and Tsien RW. Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices see comments. Neuron 22: 395-409, 1999.
120. Liu G and Tsien RW. Properties of synaptic transmission at single hippocampal synaptic boutons. Nature 375: 404-408, 1995.
121. Lynch BA, Lambeng N, Nocka K, Kensel-Hammes P, Bajjalieh SM, Matagne A, and Fuks B. The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci USA 101: 9861-9866, 2004.
122. Mainen ZF, Malinow R, and Svoboda K. Synaptic calcium transients in single spines indicate that NMDA receptors are not saturated. Nature 399: 151-155, 1999.
123. Malinow R and Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126, 2002.
124. Manolson MF, Wu B, Proteau D, Taillon BE, Roberts BT, Hoyt MA, and Jones EW. STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H(+)-ATPase subunit Vph1p. J Biol Chem 269: 14064-14074, 1994.
125. Marc RE, Liu WL, Kalloniatis M, Raiguel SF, and van Haesendonck E. Patterns of glutamate immunoreactivity in the goldfish retina. J Neurosci 10: 4006-4034, 1990.
126. Marcaggi P, Billups D, and Attwell D. The role of glial glutamate transporters in maintaining the independent operation of juvenile mouse cerebellar parallel fibre synapses. J Physiol 552: 89-107, 2003.
127. Maron R, Stern Y, Kanner BI, and Schuldiner S. Functional asymmetry of the amine transporter from chromaffin granules. J Biol Chem 258: 11476-11481, 1983.
128. Masson J, Darmon M, Conjard A, Chuhma N, Ropert N, Thoby-Brisson M, Foutz AS, Parrot S, Miller GM, Jorisch R, Polan J, Hamon M, Hen R, and Rayport S. Mice lacking brain/kidney phosphate-activated glutaminase have impaired glutamatergic synaptic transmission, altered breathing, disorganized goal-directed behavior and die shortly after birth. J Neurosci 26: 4660-4671, 2006.
129. Mathews GC and Diamond JS. Neuronal glutamate uptake Contributes to GABA synthesis and inhibitory synaptic strength. J Neurosci 23: 2040-2048, 2003.
130. Maycox PR, Deckwerth T, Hell JW, and Jahn R. Glutamate uptake by brain synaptic vesicles. Energy dependence of transport and functional reconstitution in proteoliposomes. J Biol Chem 263: 15423-15428, 1988.
131. McAllister AK and Stevens CF. Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proc Natl Acad Sci USA 97: 6173-6178, 2000.
132. Miyazaki T, Fukaya M, Shimizu H, and Watanabe M. Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17: 2563-2572, 2003.
133. Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I, Daneels G, Buist A, Cik M, van der Spek P, Kass S, Meert T, D'Hooge R, Rosenmund C, and Hampson RM. Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci 26: 12055-12066, 2006.
134. Morin P, Sagne C, and Gasnier B. Functional characterization of wild-type and mutant human sialin. Embo J 23: 4560-4570, 2004.
135. Mosharov EV, Gong LW, Khanna B, Sulzer D, and Lindau M. Intracellular patch electrochemistry: regulation of cytosolic catecholamines in chromaffin cells. J Neurosci 23: 5835-5845, 2003.
136. Naito S and Ueda T. Characterization of glutamate uptake into synaptic vesicles. J Neurochem 44: 99-109, 1985.
137. Nakanishi-Matsui M and Futai M. Stochastic proton pumping ATPases: from single molecules to diverse physiological roles. IUBMB Life 58: 318-322, 2006.
138. Naves LA and Van der Kloot W. Repetitive nerve stimulation decreases the acetylcholine content of quanta at the frog neuromuscular junction. J Physiol 532: 637-647, 2001.
139. Ni B, Rosteck PR, Nadi NS, and Paul SM. Cloning and expression of a cDNA encoding a brain-specific Na+-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci USA 91: 5607-5611, 1994.
140. Oertner TG, Sabatini BL, Nimchinsky EA, and Svoboda K. Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5: 657-664, 2002.
141. Oliet SH, Piet R, and Poulain DA. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-926, 2001.
142. Otis TS and Jahr CE. Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 18: 7099-7110, 1998.
143. Otis TS, Kavanaugh MP, and Jahr CE. Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277: 1515-1518, 1997.
144. Otis TS, Wu YC, and Trussell LO. Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J Neurosci 16: 1634-1644, 1996.
145. Ozkan ED, Lee FS, and Ueda T. A protein factor that inhibits ATP-dependent glutamate and g-aminobutyric acid accumulation into synaptic vesicles: purification and initial characterization. Proc Natl Acad Sci USA 94: 4137-4142, 1997.
146. Pahner I, Holtje M, Winter S, Takamori S, Bellocchio EE, Spicher K, Laake P, Numberg B, Ottersen OP, and Ahnert-Hilger G. Functional G-protein heterotrimers are associated with vesicles of putative glutamatergic terminals: implications for regulation of transmitter uptake. Mol Cell Neurosci 23: 398-413, 2003.
147. Palmer MJ, Taschenberger H, Hull C, Tremere L, and von Gersdorff H. Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J Neurosci 23: 4831-4841, 2003.
148. Parsons RL, Calupca MA, Merriam LA, and Prior C. Empty synaptic vesicles recycle and undergo exocytosis at vesamicol-treated motor nerve terminals. J Neurophysiol 81: 2696-2700, 1999.
149. Peghini P, Janzen J, and Stoffel W. Glutamate transporter EAAC-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. Embo J 16: 3822-3832, 1997.
150. Peter D, Jimenez J, Liu Y, Kim J, and Edwards RH. The chromaffin granule and synaptic vesicle amine transporters differ in substrate recognition and sensitivity to inhibitors. J Biol Chem 269: 7231-7237, 1994.
151. Peters C, Bayer MJ, Buhler S, Andersen JS, Mann M, and Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409: 581-588, 2001.
152. Picollo A and Pusch M. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436: 420-423, 2005.
153. Pothos EN, Larsen KE, Krantz DE, Liu Y-J, Haycock JW, Setlik W, Gershon ME, Edwards RH, and Sulzer D. Synaptic vesicle transporter expression regulates vesicle phenotype and quantal size. J Neurosci 20: 7297-7306, 2000.
154. Pothos EN, Mosharov E, Liu KP, Setlik W, Haburcak M, Baldini G, Gershon MD, Tamir H, and Sulzer D. Stimulation-dependent regulation of the pH, volume and quantal size of bovine and rodent secretory vesicles. J Physiol 542: 453-476, 2002.
155. Pow DV and Barnett NL. Developmental expression of excitatory amino acid transporter 5: a photoreceptor and bipolar cell glutamate transporter in rat retina. Neurosci Lett 280: 21-24, 2000.
156. Pow DV and Crook DK. Direct immunocytochemical evidence for the transfer of glutamine from glial cells to neurons: use of specific antibodies directed against the dstereoisomers of glutamate and glutamine. Neuroscience 70: 295-302, 1996.
157. Pow DV and Robinson SR. Glutamate in some retinal neurons is derived solely from glia. Neurosci 60: 355-366, 1994.
158. Prado VF, Martins-Silva C, de Castro BM, and Lima. Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 51, 2006.
159. Price GD and Trussell LO. Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J Neurosci 26: 11432-11436, 2006.
160. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, and Rothstein JD. Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS. J Neurosci 27: 6607-6619, 2007.
161. Rizzoli SO and Betz WJ. Synaptic vesicle pools. Nat Rev Neurosci 6: 57-69, 2005.
162. Rossi DJ, Oshima T, and Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403: 316-321, 2000.
163. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, and al e. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16: 675-686, 1996.
164. Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, Nash N, and Kuncl RW. Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725, 1994.
165. Rothstein JD and Tabakoff B. Alteration of striatal glutamate release after glutamine synthetase inhibition. J Neurochem 43: 1438-1446, 1984.
166. Sandoval GM, Duerr JS, Hodgkin J, Rand JB, and Ruvkun G. A genetic interaction between the vesicular acetylcholine transporter VAChT/UNC-17 and synaptobrevin/SNB-1 in C. elegans. Nat Neurosci 9: 599-601, 2006.
167. Sarantis M, Ballerini L, Miller B, Silver RA, Edwards M, and Attwell D. Glutamate uptake from the synaptic cleft does not shape the decay of the non-NMDA component of the synaptic current. Neuron 11: 541-549, 1993.
168. Schafer MK, Varoqui H, Defamie N, Weihe E, and Erickson JD. Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J Biol Chem 277: 50734-50748, 2002.
169. Scheel O, Zdebik AA, Lourdel S, and Jentsch TJ. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436: 424-427, 2005.
170. Sepkuty JP, Cohen AS, Eccles C, Rafiq A, Behar K, Ganel R, Coulter DA, and Rothstein JD. A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. J Neurosci 22: 6372-6379, 2002.
171. Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, Yumoto N, and Nakajima T. DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53: 195-201, 1998.
172. Shupliakov O, Atwood HL, Ottersen OP, Storm-Mathisen J, and Brodin L. Presynaptic glutamate levels in tonic and phasic motor axons correlate with properties of synaptic release. J Neurosci 15: 7168-7180, 1995.
173. Smear MC, Tao HW, Staub W, Orger MB, Gosse NJ, Liu Y, Takahashi K, Poo MM, and Baier H. Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish. Neuron 53: 65-77, 2007.
174. Song H-j, Ming G-l, Fon E, Bellocchio E, Edwards RH, and Poo M-m. Expression of a putative vesicular acetylcholine transporter facilitates quantal transmitter packaging. Neuron 18: 815-826, 1997.
175. Spacek J. Three-dimensional analysis of dendritic spines. III. Glial sheath. Anat Embryol (Berl) 171: 245-252, 1985.
176. Steinert JR, Kuromi H, Hellwig A, Knirr M, Wyatt AW, Kidokoro Y, and Schuster CM. Experience-dependent formation and recruitment of large vesicles from reserve pool. Neuron 50: 723-733, 2006.
177. Stobrawa SM, Breiderhoff T, Takamori S, Engel D, Schweizer M, Zdebik AA, Bösl MR, Ruether K, Jahn H, Draguhn A, Jahn R, and Jentsch TJ. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29: 185-196, 2001.
178. Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FM, and Ottersen OP. First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301: 517-520, 1983.
179. Sullivan R, Rauen T, Fischer F, Wiessner M, Grewer C, Bicho A, and Pow DV. Cloning, transport properties, and differential localization of two splice variants of GLT-1 in the rat CNS: implications for CNS glutamate homeostasis. Glia 45: 155-169, 2004.
180. Sulzer D and Pothos EN. Regulation of quantal size by presynaptic mechanisms. Rev Neurosci 11: 159-212, 2000.
181. Tabb JS, Kish PE, Van Dyke R, and Ueda T. Glutamate transport into synaptic vesicles. J Biol Chem 267: 15412-15418, 1992.
182. Takamori S, Malherbe P, Broger C, and Jahn R. Molecular cloning and functional characterization of human vesicular glutamate transporter 3. EMBO Rep 3: 798-803, 2002.
183. Takamori S, Rhee JS, Rosenmund C, and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407: 189-194, 2000.
184. Takamori S, Rhee JS, Rosenmund C, and Jahn R. Identification of differentiationassociated brain-specific phosphate transporter as a second vesicular glutamate transporter. J Neurosci 21: RC182, 2001.
185. Takayasu Y, Iino M, Kakegawa W, Maeno H, Watase K, Wada K, Yanagihara D, Miyazaki T, Komine O, Watanabe M, Tanaka K, and Ozawa S. Differential roles of glial and neuronal glutamate transporters in Purkinje cell synapses. J Neurosci 25: 8788-8793, 2005.
186. Takayasu Y, Iino M, Shimamoto K, Tanaka K, and Ozawa S. Glial glutamate transporters maintain one-to-one relationship at the climbing fiber-Purkinje cell synapse by preventing glutamate spillover. J Neurosci 26: 6563-6572, 2006.
187. Tamir H, Liu KP, Adlersberg M, Hsiung SC, and Gershon MD. Acidification of serotonin-containing secretory vesicles induced by a plasma membrane calcium receptor. J Biol Chem 271: 6441-6450, 1996.
188. Tamura Y, Ozkan ED, Bole DG, and Ueda T. IPF, a vesicular uptake inhibitory protein factor, can reduce the Ca(2+)-dependent, evoked release of glutamate, GABA and serotonin. J Neurochem 76: 1153-1164, 2001.
189. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, and Wada K. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276: 1699-1702, 1997.
190. Tanaka K, Watase K, Manabe T, Yamada K, Watanabe M, Takahashi K, Iwama H, Nishikawa T, Ichihara N, Kikuchi T, Okuyama S, Kawashima N, Hori S, Takimoto M, and Wada K. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276: 1699-1702, 1997.
191. Tani H, Bandrowski AE, Parada I, Wynn M, Huguenard JR, Prince DA, and Reimer RJ. Modulation of epileptiform activity by glutamine and system A transport in a model of post-traumatic epilepsy. Neurobiol Dis 25: 230-238, 2007.
192. Theodosis DT and Poulain DA. Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus. Neuroscience 57: 501-535, 1993.
193. Tong G and Jahr CE. Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13: 1195-1203, 1994.
194. Torres GE and Amara SG. Glutamate and monoamine transporters: new visions of form and function. Curr Opin Neurobiol 17: 304-312, 2007.
195. Travis ER, Wang YM, Michael DJ, Caron MG, and Wightman RM. Differential quantal release of histamine and 5-hydroxytryptamine from mast cells of vesicular monoamine transporter 2 knockout mice. Proc Natl Acad Sci USA 97: 162-167, 2000.
196. Trussell LO and Fischbach GD. Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3: 209-218, 1989.
197. Van der Kloot W. Loading and recycling of synaptic vesicles in the Torpedo electric organ and the vertebrate neuromuscular junction. Prog Neurobiol 71: 269-303, 2003.
198. Van der Kloot W, Colasante C, Cameron R, and Molgo J. Recycling and refilling of transmitter quanta at the frog neuromuscular junction. J Physiol 523 Pt 1: 247-258, 2000.
199. Varoqui H and Erickson JD. Active transport of acetylcholine by the human vesicular acetylcholine transporter. J Biol Chem 271: 27229-27232, 1996.
200. Varoqui H, Schafer MK-H, Zhu H, Weihe E, and Erickson JD. Identification of the differentiation-associated Na+/Pi transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22: 142-155, 2002.
201. Ventura R and Harris KM. Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci 19: 6897-6906., 1999.
202. Verheijen FW, Verbeek E, Aula N, Beerens CE, Havelaar AC, Joosse M, Peltonen L, Aula P, Galjaard H, van der Spek PJ, and Mancini GM. A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nature Genetics 23: 462-465, 1999.
203. Veruki ML, Morkve SH, and Hartveit E. Activation of a presynaptic glutamate transporter regulates synaptic transmission through electrical signaling. Nat Neurosci 9: 1388-1396, 2006.
204. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, and Edwards RH. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51: 71-84, 2006.
205. Wadiche JI, Amara SG, and Kavanaugh MP. Ion fluxes associated with excitatory amino acid transport. Neuron 15: 721-728, 1995.
206. Wadiche JI, Arriza JL, Amara SG, and Kavanaugh MP. Kinetics of a human glutamate transporter. Neuron 14: 1019-1027, 1995.
207. Wadiche JI and Jahr CE. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32: 301-313, 2001.
208. Wadiche JI and Jahr CE. Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nat Neurosci 8: 1329-1334, 2005.
209. Wadiche JI and Kavanaugh MP. Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J Neurosci 18: 7650-7661, 1998.
210. Wallen-Mackenzie A, Gezelius H, Thoby-Brisson M, Nygard A, Enjin A, Fujiyama F, Fortin G, and Kullander K. Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J Neurosci 26: 12294-12307, 2006.
211. Wang X, Li Y, Engisch KL, Nakanishi ST, Dodson SE, Miller GW, Cope TC, Pinter MJ, and Rich MM. Activity-dependent presynaptic regulation of quantal size at the mammalian neuromuscular junction in vivo. J Neurosci 25: 343-351, 2005.
212. Watase K, Hashimoto K, Kano M, Yamada K, Watanabe M, Inoue Y, Okuyama S, Sakagawa T, Ogawa S, Kawashima N, Hori S, Takimoto M, Wada K, and Tanaka K. Motor discoordination and increased susceptibility to cerebellar injury in GLAST mutant mice. Eur J Neurosci 10: 976-988, 1998.
213. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, and Liu G. Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25: 6221-6234, 2005.
214. Winkler BS, Kapousta-Bruneau N, Arnold MJ, and Green DG. Effects of inhibiting glutamine synthetase and blocking glutamate uptake on b-wave generation in the isolated rat retina. Vis Neurosci 16: 345-353, 1999.
215. Winter S, Brunk I, Walther DJ, Holtje M, Jiang M, Peter JU, Takamori S, Jahn R, Birnbaumer L, and Ahnert-Hilger G. Galphao2 regulates vesicular glutamate transporter activity by changing its chloride dependence. J Neurosci 25: 4672-4680, 2005.
216. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, and Rosenmund C. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci USA 101: 7158-7163, 2004.
217. Wolosker H, de Souza DO, and de Meis L. Regulation of glutamate transport into synaptic vesicles by chloride and proton gradient. J Biol Chem 271: 11726-11731, 1996.
218. Wreden CC, Wlizla M, and Reimer RJ. Varied mechanisms underlie the free sialic acid storage disorders. J Biol Chem 280: 1408-1416, 2005.
219. Wu XS, Xue L, Mohan R, Paradiso K, Gillis KD, and Wu LG. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. J Neurosci 27: 3046-3056, 2007.
220. Yamada K, Watanabe M, Shibata T, Tanaka K, Wada K, and Inoue Y. EAAT4 is a postsynaptic glutamate transporter at Purkinje cell synapses. Neuroreport 7: 2013-2017, 1996.
221. Yamashita T, Ishikawa T, and Takahashi T. Developmental increase in vesicular glutamate content does not cause saturation of AMPA receptors at the calyx of held synapse. J Neurosci 23: 3633-3638, 2003.
222. Yelamanchili SV, Pendyala G, Brunk I, Darna M, Albrecht U, and Ahnert-Hilger G. Differential sorting of the vesicular glutamate transporter 1 into a defined vesicular pool is regulated by light signaling involving the clock gene Period2. J Biol Chem 281: 15671-15679, 2006.
223. Zerangue N and Kavanaugh MP. Flux coupling in a neuronal glutamate transporter. Nature 383: 634-637, 1996.
224. Zhang B, Ganetzky B, Bellen HJ, and Murthy VN. Tailoring uniform coats for synaptic vesicles during endocytosis. Neuron 23: 419-422, 1999.
225. Zhang B, Koh YH, Beckstead RB, Budnik V, Ganetzky B, and Bellen HJ. Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21: 1465-1475, 1998.
226. Zhou Q, Petersen CCH, and Nicoll RA. Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J Physiol 525: 195-206, 2000.
227. Zimmermann H and Denston CR. Recycling of synaptic vesicles in the cholinergic synapses of the Torpedo electric organ during induced transmitter release. Neuroscience 2: 695-714, 1977.