Vesicular uptake and exocytosis of L-aspartate is independent of sialin

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 1264-1274

  Morland, Cecilie ^a   Nordengen, Kaja ^a   Larsson, Max ^a,b   Prolo, Laura M ^c   Farzampour, Zoya ^c   Reimer, Richard J ^c   Gundersen, Vidar ^a,d  

^a UNIVERSITY OF OSLO   (Norway)

^b KAROLINSKA INSTITUTE   (Sweden)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Excitatory amino acid transporters; Synaptic transmission; VRAC

Indexed keywords

AMINO ACID TRANSPORTER; ASPARTIC ACID; GLUTAMIC ACID; LIPOSOME; PROTEIN; SIALIN; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANIMAL TISSUE; ARTICLE; BRAIN; BRAIN SLICE; CONTROLLED STUDY; CORPUS STRIATUM; DEPOLARIZATION; ENTORHINAL CORTEX; EXOCYTOSIS; FRONTAL CORTEX; HIPPOCAMPUS; MALE; MOUSE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE;

ADENOSINE TRIPHOSPHATE; ANIMALS; ASPARTIC ACID; BRAIN; EXOCYTOSIS; MALE; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROTRANSMITTER AGENTS; ORGANIC ANION TRANSPORTERS; PC12 CELLS; RATS; RATS, WISTAR; SYMPORTERS; SYNAPTIC VESICLES;

EID: 84874607595     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-206300     Document Type: Article

References (80)

1. Nadler, J. V., Vaca, K. W., White, W. F., Lynch, G. S., and Cotman, C. W. (1976) Aspartate and glutamate as possible transmitters of excitatory hippocampal afferents. Nature 260, 538-540
2. Wiklund, L., Toggenburger, G., and Cuenod, M. (1982) Aspartate: possible neurotransmitter in cerebellar climbing fibers. Science 216, 78-80 (Pubitemid 12155912)
3. Nadler, J. V. (2011) Aspartate release and signalling in the hippocampus. Neurochem. Res. 36, 668-676
4. Gundersen, V. (2008) Co-localization of excitatory and inhibitory transmitters in the brain. Acta Neurol. Scand. 188(Suppl.), 29-33 (Pubitemid 351595270)
5. Gundersen, V., and Storm-Mathisen J. (2000) Aspartate-neurochemical evidence for a transmitter role. In Handbook of Chemical Neuroanatomy (Ottersen, O. P., and Storm-Mathisen, J., eds) pp. 45-62, Elsevier, Amsterdam
6. Curras, M. C., and Dingledine, R. (1992) Selectivity of amino acid transmitters acting at N-methyl-D-aspartate and amino-3-hydroxy-5-methyl-4- isoxazolepropionate receptors. Mol. Pharmacol. 41, 520-526
7. Zhang, X., and Nadler, J. V. (2009) Postsynaptic response to stimulation of the Schaffer collaterals with properties similar to those of synaptosomal aspartate release. Brain Res. 1295, 13-20
8. Fleck, M. W., Henze, D. A., Barrionuevo, G., and Palmer, A. M. (1993) Aspartate and glutamate mediate excitatory synaptic transmission in area CA1 of the hippocampus. J. Neurosci. 13, 3944-3955 (Pubitemid 23264378)
9. Christensen, H., Fykse, E. M., and Fonnum, F. (1991) Inhibition of gamma-aminobutyrate and glycine uptake into synaptic vesicles. Eur. J. Pharmacol. 207, 73-79
10. Christensen, H., Fykse, E. M., and Fonnum, F. (1990) Uptake of glycine into synaptic vesicles isolated from rat spinal cord. J. Neurochem. 54, 1142-1147
11. Fykse, E. M., Iversen, E. G., and Fonnum, F. (1992) Inhibition of L-glutamate uptake into synaptic vesicles. Neurosci. Lett. 135, 125-128
12. Naito, S., and Ueda, T. (1983) Adenosine triphosphate-dependent uptake of glutamate into protein I-associated synaptic vesicles. J. Biol. Chem. 258, 696-699 (Pubitemid 13139315)
13. Maycox, P. R., Deckwerth, T., Hell, J. W., and Jahn, R. (1988) Glutamate uptake by brain synaptic vesicles: energy dependence of transport and functional reconstitution in proteoliposomes. J. Biol. Chem. 263, 15423-15428
14. Verheijen, F. W., Verbeek, E., Aula, N., Beerens, C. E., Havelaar, A. C., Joosse, M., Peltonen, L., Aula, P., Galjaard, H., van der Spek, P. J., and Mancini, G. M. (1999) A new gene, encoding an anion transporter, is mutated in sialic acid storage diseases. Nat. Genet. 23, 462-465
15. Miyaji, T., Echigo, N., Hiasa, M., Senoh, S., Omote, H., and Moriyama, Y. (2008) Identification of a vesicular aspartate transporter. Proc. Natl. Acad. Sci. U. S. A. 105, 11720-11724
16. Prolo, L. M., Vogel, H., and Reimer, R. J. (2009) The lysosomal sialic acid transporter sialin is required for normal CNS myelination. J. Neurosci. 29, 15355-15365
17. Erickson, J. D., Masserano, J. M., Barnes, E. M., Ruth, J. A., and Weiner, N. (1990) Chloride ion increases [3H]dopamine accumulation by synaptic vesicles purified from rat striatum: inhibition by thiocyanate ion. Brain Res. 516, 155-160 (Pubitemid 20189215)
18. Fykse, E. M., Christensen, H., and Fonnum, F. (1989) Comparison of the properties of gamma-aminobutyric acid and L-glutamate uptake into synaptic vesicles isolated from rat brain. J. Neurochem. 52, 946-951 (Pubitemid 19067558)
19. Bellocchio, E. E., Reimer, R. J., Fremeau, R. T., Jr., and Edwards, R. H. (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289, 957-960 (Pubitemid 30659949)
20. Wreden, C. C., Wlizla, M., and Reimer, R. J. (2005) Varied mechanisms underlie the free sialic acid storage disorders. J. Biol. Chem. 280, 1408-1416
21. Gundersen, V., Ottersen, O. P., and Storm-Mathisen, J. (1991) Aspartate- and glutamate-like immunoreactivities in rat hippocampal slices: depolarization-induced redistribution and effects of precursors. Eur. J. Neurosci. 3, 1281-1299
22. Gundersen, V., Chaudhry, F. A., Bjaalie, J. G., Fonnum, F., Ottersen, O. P., and Storm-Mathisen, J. (1998) Synaptic vesicular localization and exocytosis of L-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J. Neurosci. 18, 6059-6070 (Pubitemid 28373215)
23. Holten, A. T., Morland, C., Nordengen, K., and Gundersen, V. (2008) Vesicular release of l- and d-aspartate from hippocampal nerve terminals: immunogold evidence. Open Neurosci. J. 2, 51-58
24. Bergersen, L. H., Storm-Mathisen, J., and Gundersen, V. (2008) Immunogold quantification of amino acids and proteins in complex subcellular compartments. Nat. Protoc. 3, 144-152
25. Gundersen, V., Danbolt, N. C., Ottersen, O. P., and Storm-Mathisen, J. (1993) Demonstration of glutamate/aspartate uptake activity in nerve endings by use of antibodies recognizing exogenous d-aspartate. Neuroscience 57, 97-111 (Pubitemid 23325637)
26. Gundersen, V., Fonnum, F., Ottersen, O. P., and Storm-Mathisen, J. (2001) Redistribution of neuroactive amino acids in hippocampus and striatum during hypoglycemia: a quantitative immunogold study. J. Cereb. Blood Flow Metab 21, 41-51 (Pubitemid 32016838)
27. Gundersen, V., Holten, A. T., and Storm-Mathisen, J. (2004) GABAergic synapses in hippocampus exocytose aspartate on to NMDA receptors: quantitative immunogold evidence for cotransmission. Mol. Cell Neurosci. 26, 156-165 (Pubitemid 38581031)
28. Ottersen, O. P. (1987) Postembedding light- and electron microscopic immunocytochemistry of amino acids: description of a new model system allowing identical conditions for specificity testing and tissue processing. Exp. Brain Res. 69, 167-174 (Pubitemid 18012826)
29. Ottersen, O. P., Zhang, N., and Walberg, F. (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46, 519-534
30. Larsson, M., Sawada, K., Morland, C., Hiasa, M., Ormel, L., Moriyama, Y., and Gundersen, V. (2012) Functional and anatomical identification of a vesicular transporter mediating neuronal ATP release. Cereb. Cortex 22, 1203-1214
31. Larsson, M., and Broman, J. (2005) Different basal levels of CaMKII phosphorylated at Thr286/287 at nociceptive and low-threshold primary afferent synapses. Eur. J. Neurosci. 21, 2445-2458 (Pubitemid 40813926)
32. Ogita, K., Hirata, K., Bole, D. G., Yoshida, S., Tamura, Y., Leckenby, A. M., and Ueda, T. (2001) Inhibition of vesicular glutamate storage and exocytotic release by Rose Bengal. J. Neurochem. 77, 34-42 (Pubitemid 32245077)
33. Fremeau, R. T., Jr., Voglmaier, S., Seal, R. P., and Edwards, R. H. (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci. 27, 98-103 (Pubitemid 38167332)
34. Holten, A. T., and Gundersen, V. (2008) Glutamine as a precursor for transmitter glutamate, aspartate and GABA in the cerebellum: a role for phosphate-activated glutaminase. J. Neurochem. 104, 1032-1042 (Pubitemid 351143652)
35. Morland, C., Nordengen, K., and Gundersen, V. (2012) Valproate causes reduction of the excitatory amino acid aspartate in nerve terminals. Neurosci. Lett. 527, 100-104
36. Longuemare, M. C., and Swanson, R. A. (1995) Excitatory amino acid release from astrocytes during energy failure by reversal of sodium-dependent uptake. J. Neurosci. Res. 40, 379-386
37. Roettger, V., and Lipton, P. (1996) Mechanism of glutamate release from rat hippocampal slices during in vitro ischemia. Neuroscience 75, 677-685 (Pubitemid 26377040)
38. Jabaudon, D., Scanziani, M., Gahwiler, B. H., and Gerber, U. (2000) Acute decrease in net glutamate uptake during energy deprivation. Proc. Natl. Acad. Sci. U. S. A. 97, 5610-5615 (Pubitemid 30313766)
39. Phillis, J. W., and O'Regan, M. H. (2000) Hyperglycemia and extracellular glutamate in the ischemic brain. Stroke 31, 1462-1463 (Pubitemid 30351276)
40. Marcaggi, P., Hirji, N., and Attwell, D. (2005) Release of l-aspartate by reversal of glutamate transporters. Neuropharmacology 49, 843-849 (Pubitemid 41483890)
41. Phillis, J. W., Smith-Barbour, M., Perkins, L. M., and O'Regan, M. H. (1994) Characterization of glutamate, aspartate, and GABA release from ischemic rat cerebral cortex. Brain Res. Bull. 34, 457-466 (Pubitemid 24180630)
42. Phillis, J. W., Ren, J., and O'Regan, M. H. (2000) Inhibition of Na(+)/H(+) exchange by 5-(N-ethyl-N-isopropyl)-amiloride reduces free fatty acid efflux from the ischemic reperfused rat cerebral cortex. Brain Res. 884, 155-162
43. Rossi, D. J., Oshima, T., and Attwell, D. (2000) Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403, 316-321 (Pubitemid 30062388)
44. Seki, Y., Feustel, P. J., Keller, R. W., Jr., Tranmer, B. I., and Kimelberg, H. K. (1999) Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 30, 433-440 (Pubitemid 29071814)
45. Shimamoto, K., Sakai, R., Takaoka, K., Yumoto, N., Nakajima, T., Amara, S. G., and Shigeri, Y. (2004) Characterization of novel l-threo-beta- benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol. Pharmacol. 65, 1008-1015 (Pubitemid 38420507)
46. Omelchenko, A., Bouchard, R., Le, H. D., Choptiany, P., Visen, N., Hnatowich, M., and Hryshko, L. V. (2003) Inhibition of canine (NCX1.1) and Drosophila (CALX1.1) Na(+)-Ca(2+) exchangers by 7-chloro-3,5-dihydro-5-phenyl- 1H-4,1-benzothiazepine-2-one (CGP-37157). J. Pharmacol. Exp. Ther. 306, 1050-1057 (Pubitemid 37025313)
47. Sobolevsky, A. I., and Khodorov, B. I. (1999) Blockade of NMDA channels in acutely isolated rat hippocampal neurons by the Na+/Ca2+ exchange inhibitor KB-R7943. Neuropharmacology 38, 1235-1242 (Pubitemid 29292411)
48. Kraft, R. (2007) The Na+/Ca2+ exchange inhibitor KB-R7943 potently blocks TRPC channels. Biochem. Biophys. Res. Commun. 361, 230-236 (Pubitemid 47102290)
49. Pezier, A., Bobkov, Y. V., and Ache, B. W. (2009) The Na+/Ca2+ exchanger inhibitor, KB-R7943, blocks a nonselective cation channel implicated in chemosensory transduction. J. Neurophysiol. 101, 1151-1159
50. Zhang, Y., Zhang, H., Feustel, P. J., and Kimelberg, H. K. (2008) DCPIB, a specific inhibitor of volume regulated anion channels (VRACs), reduces infarct size in MCAo and the release of glutamate in the ischemic cortical penumbra. Exp. Neurol. 210, 514-520
51. Feustel, P. J., Jin, Y., and Kimelberg, H. K. (2004) Volume-regulated anion channels are the predominant contributors to release of excitatory amino acids in the ischemic cortical penumbra. Stroke 35, 1164-1168 (Pubitemid 38543537)
52. Mongin, A. A., and Kimelberg, H. K. (2005) ATP regulates anion channel-mediated organic osmolyte release from cultured rat astrocytes via multiple Ca2+-sensitive mechanisms. Am. J. Physiol. Cell Physiol. 288, C204-C213 (Pubitemid 39658443)
53. Lewis, S. M., Lee, F. S., Todorova, M., Seyfried, T. N., and Ueda, T. (1997) Synaptic vesicle glutamate uptake in epileptic (EL) mice. Neurochem. Int. 31, 581-585 (Pubitemid 27375868)
54. Naito, S., and Ueda, T. (1985) Characterization of glutamate uptake into synaptic vesicles. J. Neurochem. 44, 99-109 (Pubitemid 15190740)
55. Zhou, M., Peterson, C. L., Lu, Y. B., and Nadler, J. V. (1995) Release of glutamate and aspartate from CA1 synaptosomes: selective modulation of aspartate release by ionotropic glutamate receptor ligands. J. Neurochem. 64, 1556-1566
56. Peterson, C. L., Thompson, M. A., Martin, D., and Nadler, J. V. (1995) Modulation of glutamate and aspartate release from slices of hippocampal area CA1 by inhibitors of arachidonic acid metabolism. J. Neurochem. 64, 1152-1160
57. Nadler, J. V., White, W. F., Vaca, K. W., Perry, B. W., and Cotman, C. W. (1978) Biochemical correlates of transmission mediated by glutamate and aspartate. J. Neurochem. 31, 147-155 (Pubitemid 8390987)
58. Kadota, K., and Kadota, T. (1973) Isolation of coated vesicles, plain synaptic vesicles, and flocculent material from a crude synaptosome fraction of guinea pig whole brain. J. Cell Biol. 58, 135-151
59. Huttner, W. B., Schiebler, W., Greengard, P., and De, C. P. (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96, 1374-1388 (Pubitemid 13029640)
60. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Gronborg, M., Riedel, D., Urlaub, H., Schenck, S., Brugger, B., Ringler, P., Muller, S. A., Rammner, B., Grater, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmuller, H., Heuser, J., Wieland, F., and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831-846 (Pubitemid 44716256)
61. Aula, N., Kopra, O., Jalanko, A., and Peltonen, L. (2004) Sialin expression in the CNS implicates extralysosomal function in neurons. Neurobiol. Dis. 15, 251-261 (Pubitemid 38296756)
62. Yarovaya, N., Schot, R., Fodero, L., McMahon, M., Mahoney, A., Williams, R., Verbeek, E., de, B. A., Hampson, M., van der, S. P., Stubbs, A., Masters, C. L., Verheijen, F. W., Mancini, G. M., and Venter, D. J. (2005) Sialin, an anion transporter defective in sialic acid storage diseases, shows highly variable expression in adult mouse brain, and is developmentally regulated. Neurobiol. Dis. 19, 351-365 (Pubitemid 40968049)
63. Phillis, J. W., Song, D., and O'Regan, M. H. (1997) Inhibition by anion channel blockers of ischemia-evoked release of excitotoxic and other amino acids from rat cerebral cortex. Brain Res. 758, 9-16 (Pubitemid 27310636)
64. Phillis, J. W., Song, D., and O'Regan, M. H. (1998) Tamoxifen, a chloride channel blocker, reduces glutamate and aspartate release from the ischemic cerebral cortex. Brain Res. 780, 352-355 (Pubitemid 28082924)
65. Furness, D. N., Dehnes, Y., Akhtar, A. Q., Rossi, D. J., Hamann, M., Grutle, N. J., Gundersen, V., Holmseth, S., Lehre, K. P., Ullensvang, K., Wojewodzic, M., Zhou, Y., Attwell, D., and Danbolt, N. C. (2008) A quantitative assessment of glutamate uptake into hippocampal synaptic terminals and astrocytes: new insights into a neuronal role for excitatory amino acid transporter 2 (EAAT2). Neuroscience 157, 80-94
66. Szatkowski, M., Barbour, B., and Attwell, D. (1990) Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348, 443-446 (Pubitemid 120015084)
67. Phillis, J. W., Ren, J., and O'Regan, M. H. (2000) Transporter reversal as a mechanism of glutamate release from the ischemic rat cerebral cortex: studies with DL-threo-beta-benzyloxyaspartate. Brain Res. 868, 105-112 (Pubitemid 30332348)
68. Raiteri, L., Zappettini, S., Milanese, M., Fedele, E., Raiteri, M., and Bonanno, G. (2007) Mechanisms of glutamate release elicited in rat cerebrocortical nerve endings by 'pathologically' elevated extraterminal K+ concentrations. J. Neurochem. 103, 952-961 (Pubitemid 47568713)
69. Cavallero, A., Marte, A., and Fedele, E. (2009) L-aspartate as an amino acid neurotransmitter: mechanisms of the depolarization-induced release from cerebrocortical synaptosomes. J. Neurochem. 110, 924-934
70. Nadler, J. V., Martin, D., Bustos, G. A., Burke, S. P., and Bowe, M. A. (1990) Regulation of glutamate and aspartate release from the Schaffer collaterals and other projections of CA3 hippocampal pyramidal cells. Prog. Brain Res. 83, 115-130 (Pubitemid 20205275)
71. Burke, S. P., and Nadler, J. V. (1988) Regulation of glutamate and aspartate release from slices of the hippocampal CA1 area: effects of adenosine and baclofen. J. Neurochem. 51, 1541-1551 (Pubitemid 18264377)
72. Szerb, J. C. (1988) Changes in the relative amounts of aspartate and glutamate released and retained in hippocampal slices during stimulation. J. Neurochem. 50, 219-224 (Pubitemid 18023502)
73. Roisin, M. P., Brassart, J. L., Charton, G., Crepel, V., and Ben, A. Y. (1991) A new method for the measurement of endogenous transmitter release in localized regions of hippocampal slices. J. Neurosci. Methods 37, 183-189
74. Bradford, S. E., and Nadler, J. V. (2004) Aspartate release from rat hippocampal synaptosomes. Neuroscience 128, 751-765 (Pubitemid 39298428)
75. Girault, J. A., Barbeito, L., Spampinato, U., Gozlan, H., Glowinski, J., and Besson, M. J. (1986) In vivo release of endogenous amino acids from the rat striatum: further evidence for a role of glutamate and aspartate in corticostriatal neurotransmission. J. Neurochem. 47, 98-106 (Pubitemid 16069177)
76. Paulsen, R. E., and Fonnum, F. (1989) Role of glial cells for the basal and Ca2+-dependent K+-evoked release of transmitter amino acids investigated by microdialysis. J. Neurochem. 52, 1823-1829 (Pubitemid 19140769)
77. Zappettini, S., Grilli, M., Salamone, A., Fedele, E., and Marchi, M. (2010) Pre-synaptic nicotinic receptors evoke endogenous glutamate and aspartate release from hippocampal synaptosomes by way of distinct coupling mechanisms. Br. J. Pharmacol. 161, 1161-1171
78. McMahon, H. T., Foran, P., Dolly, J. O., Verhage, M., Wiegant, V. M., and Nicholls, D. G. (1992) Tetanus toxin and botulinum toxins type A and B inhibit glutamate, gamma-aminobutyric acid, aspartate, and met-enkephalin release from synaptosomes: clues to the locus of action. J. Biol. Chem. 267, 21338-21343
79. Wang, L., and Nadler, J. V. (2007) Reduced aspartate release from rat hippocampal synaptosomes loaded with Clostridial toxin light chain by electroporation: evidence for an exocytotic mechanism. Neurosci. Lett. 412, 239-242 (Pubitemid 46109149)
80. Brustovetsky, T., Brittain, M. K., Sheets, P. L., Cummins, T. R., Pinelis, V., and Brustovetsky, N. (2011) KB-R7943, an inhibitor of the reverse Na+/Ca2+ exchanger, blocks N-methyl-d-aspartate receptor and inhibits mitochondrial complex I. Br. J. Pharmacol. 162, 255-270