Mechanisms of substrate transport-induced clustering of a glial glutamate transporter GLT-1 in astroglial-neuronal cultures

European Journal of Neuroscience

Volumn 28, Issue 9, 2008, Pages 1719-1730

  Nakagawa, Takayuki ^a   Otsubo, Yasuto ^a   Yatani, Yumi ^a   Shirakawa, Hisashi ^a   Kaneko, Shuji ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Astrocyte; Endocytosis; Na+; Rat; Trafficking

Indexed keywords

3 [3 [4 (TRIFLUOROMETHYL)BENZOYLAMINO]BENZYLOXY]ASPARTATE; ASPARTIC ACID; CALCIUM; DICARBOXYLIC ACID; DIHYDROKAINIC ACID; ENHANCED GREEN FLUORESCENT PROTEIN; GLUTAMIC ACID; GLUTAMIC ACID DERIVATIVE; GRAMICIDIN; IONOPHORE; IONOTROPIC RECEPTOR ANTAGONIST; METABOTROPIC RECEPTOR ANTAGONIST; MONENSIN; OUABAIN; SODIUM; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ADENOVIRUS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CALCIUM SIGNALING; CELL CULTURE; CELL MIGRATION; CELL SURFACE; EMBRYO; ENDOCYTOSIS; ENDOSOME; FEMALE; FETUS; GLIA; HUMAN; HUMAN CELL; LYSOSOME; MEMBRANE DEPOLARIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SODIUM TRANSPORT; VIRUS INFECTION;

ANIMALS; ASTROCYTES; CELL MEMBRANE; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOCYTOSIS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMIC ACID; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; IONOPHORES; NEURONS; PROTEIN TRANSPORT; PROTEINS; RATS; RATS, WISTAR; RECOMBINANT FUSION PROTEINS; SODIUM; SODIUM CHANNELS; TRANSPORT VESICLES;

EID: 54849417590     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06494.x     Document Type: Article

References (67)

1. Akasaki, K., Michihara, A., Fujiwara, Y., Mibuka, K. Tsuji, H. (1996) Biosynthetic transport of a major lysosome-associated membrane glycoprotein 2, lamp-2: a significant fraction of newly synthesized lamp-2 is delivered to lysosomes by way of early endosomes. J. Biochem., 120, 1088 1094.
2. Apparsundaram, S., Schroeter, S., Giovanetti, E. Blakely, R.D. (1998) Acute regulation of norepinephrine transport: II. PKC-modulated surface expression of human norepinephrine transporter proteins. J. Pharmacol. Exp. Ther., 287, 744 751.
3. 2+entry in cultured neurons and astrocytes. Biochem. Biophys. Res. Commun., 279, 354 357.
4. Aronica, E., Gorter, J.A., Ijlst-Keizers, H., Rozemuller, A.J., Yankaya, B., Leenstra, S. Troost, D. (2003) Expression and functional role of mGluR3 and mGluR5 in human astrocytes and glioma cells: opposite regulation of glutamate transporter proteins. Eur. J. Neurosci., 17, 2106 2118.
5. Aschner, M., Sonnewald, U. Tan, K.H. (2002) Astrocyte modulation of neurotoxic injury. Brain Pathol., 12, 475 481.
6. Beart, P.M. O'Shea, R.D. (2007) Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br. J. Pharmacol., 150, 5 17.
7. Beaumont, V., Hepworth, M.B., Luty, J.S., Kelly, E. Henderson, G. (1998) Somatostatin receptor desensitization in NG108-15 cells. A consequence of receptor sequestration. J. Biol. Chem., 273, 33174 33183.
8. Beckman, M.L., Bernstein, E.M. Quick, M.W. (1999) Multiple G protein-coupled receptors initiate protein kinase C redistribution of GABA transporters in hippocampal neurons. J. Neurosci., 19, RC9.
9. Bernstein, E.M. Quick, M.W. (1999) Regulation of gamma-aminobutyric acid (GABA) transporters by extracellular GABA. J. Biol. Chem., 274, 889 895.
10. + dynamics in mouse cortical astrocytes: implications for cellular bioenergetics. Eur. J. Neurosci., 12, 3843 3853.
11. Chaudhry, F.A., Lehre, K.P., van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C. Storm-Mathisen, J. (1995) Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron, 15, 711 720.
12. Chen, N. Reith, M.E. (2004) Interaction between dopamine and its transporter: role of intracellular sodium ions and membrane potential. J. Neurochem., 89, 750 765.
13. Choi, D.W. Rothman, S.M. (1990) The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci., 13, 171 182.
14. Conti, F. Weinberg, R.J. (1999) Shaping excitation at glutamatergic synapses. Trends Neurosci., 22, 451 458.
15. Daniels, G.M. Amara, S.G. (1999) Regulated trafficking of the human dopamine transporter. Clathrin-mediated internalization and lysosomal degradation in response to phorbol esters. J. Biol. Chem., 274, 35794 35801.
16. Davis, K.E., Straff, D.J., Weinstein, E.A., Bannerman, P.G., Correale, D.M., Rothstein, J.D. Robinson, M.B. (1998) Multiple signaling pathways regulate cell surface expression and activity of the excitatory amino acid carrier 1 subtype of Glu transporter in C6 glioma. J. Neurosci., 18, 2475 2485.
17. Deken, S.L., Wang, D. Quick, M.W. (2003) Plasma membrane GABA transporters reside on distinct vesicles and undergo rapid regulated recycling. J. Neurosci., 23, 1563 1568.
18. +-dependent L-glutamate transport activity in C6 glioma cells by phorbol ester. J. Neurochem., 67, 508 516.
19. Duan, S., Anderson, C.M., Stein, B.A. Swanson, R.A. (1999) Glutamate induces rapid upregulation of astrocyte glutamate transport and cell-surface expression of GLAST. J. Neurosci., 19, 10193 10200.
20. Fagg, G.E. Foster, A.C. (1983) Amino acid neurotransmitters and their pathways in the mammalian central nervous system. Neuroscience, 9, 701 719.
21. Garlin, A.B., Sinor, A.D., Sinor, J.D., Jee, S.H., Grinspan, J.B. Robinson, M.B. (1995) Pharmacology of sodium-dependent high-affinity L-[3H]glutamate transport in glial cultures. J. Neurochem., 64, 2572 2580.
22. Gegelashvili, G. Schousboe, A. (1997) High affinity glutamate transporters: regulation of expression and activity. Mol. Pharmacol., 52, 6 15.
23. Gegelashvili, G., Robinson, M.B., Trotti, D. Rauen, T. (2001) Regulation of glutamate transporters in health and disease. Prog. Brain Res., 132, 267 286.
24. Gibson, A.E., Noel, R.J., Herlihy, J.T. Ward, W.F. (1989) Phenylarsine oxide inhibition of endocytosis: effects on asialofetuin internalization. Am. J. Physiol., 257, C182 184.
25. Guillet, B.A., Velly, L.J., Canolle, B., Masmejean, F.M., Nieoullon, A.L. Pisano, P. (2005) Differential regulation by protein kinases of activity and cell surface expression of glutamate transporters in neuron-enriched cultures. Neurochem. Int., 46, 337 346.
26. Hatten, M.E. (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J. Cell Biol., 100, 384 396.
27. Hertel, C., Coulter, S.J. Perkins, J.P. (1985) A comparison of catecholamine-induced internalization of β-adrenergic receptors and receptor-mediated endocytosis of epidermal growth factor in human astrocytoma cells. Inhibition by phenylarsine oxide. J. Biol. Chem., 260, 12547 12553.
28. Johnson, L.A., Furman, C.A., Zhang, M., Guptaroy, B. Gnegy, M.E. (2005) Rapid delivery of the dopamine transporter to the plasmalemmal membrane upon amphetamine stimulation. Neuropharmacology, 49, 750 758.
29. Kalandadze, A., Wu, Y. Robinson, M.B. (2002) Protein kinase C activation decreases cell surface expression of the GLT-1 subtype of glutamate transporter. Requirement of a carboxyl-terminal domain and partial dependence on serine 486. J. Biol. Chem., 277, 45741 45750.
30. Kosugi, T. Kawahara, K. (2006) Reversed actrocytic GLT-1 during ischemia is crucial to excitotoxic death of neurons, but contributes to the survival of astrocytes themselves. Neurochem. Res., 31, 933 943.
31. Kume, T., Nishikawa, H., Taguchi, R., Hashino, A., Katsuki, H., Kaneko, S., Minami, M., Satoh, M. Akaike, A. (2002) Antagonism of NMDA receptors by sigma receptor ligands attenuates chemical ischemia-induced neuronal death in vitro. Eur. J. Pharmacol., 29, 91 100.
32. Marshansky, V., Ausiello, D.A. Brown, D. (2002) Physiological importance of endosomal acidification: potential role in proximal tubulopathies. Curr. Opin. Nephrol. Hypertens., 11, 527 537.
33. Matute, C., Domercq, M. Sanchez-Gomez, M.V. (2006) Glutamate-mediated glial injury: mechanisms and clinical importance. Glia, 53, 212 224.
34. Melikian, H.E. (2004) Neurotransmitter transporter trafficking: endocytosis, recycling, and regulation. Pharmacol. Ther., 104, 17 27.
35. Melikian, H.E. Buckley, K.M. (1999) Membrane trafficking regulates the activity of the human dopamine transporter. J. Neurosci., 19, 7699 7710.
36. Mennerick, S., Shen, W., Xu, W., Benz, A., Tanaka, K., Shimamoto, K., Isenberg, K.E., Krause, J.E. Zorumski, C.F. (1999) Substrate turnover by transporters curtails synaptic glutamate transients. J. Neurosci., 19, 9242 9251.
37. Minelli, A., Barbaresi, P., Reimer, R.J., Edwards, R.H. Conti, F. (2001) The glial glutamate transporter GLT-1 is localized both in the vicinity of and at distance from axon terminals in the rat cerebral cortex. Neuroscience, 108, 51 59.
38. Mitani, A. Tanaka, K. (2003) Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1. J. Neurosci., 23, 7176 7182.
39. +-dependent glutamate transport activity. Neurochem. Int., 37, 147 162.
40. Ozawa, T., Nakagawa, T., Sekiya, Y., Minami, M. Satoh, M. (2004) Effect of gene transfer of GLT-1, a glutamate transporter, into the locus coeruleus by recombinant adenoviruses on morphine physical dependence in rats. Eur. J. Neurosci., 19, 221 226.
41. 2+exchanger-operated exocytotic glutamate release triggered by mild depolarization. J. Neurochem., 103, 1196 1207.
42. Perego, C., Vanoni, C., Bossi, M., Massari, S., Basudev, H., Longhi, R. Pietrini, G. (2000) The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J. Neurochem., 75, 1076 1084.
43. Pines, G., Danbolt, N.C., Bjørås, M., Zhang, Y., Bendahan, A., Eide, L., Koepsell, H., Storm-Mathisen, J., Seeberg, E. Kanner, B.I. (1992) Cloning and expression of a rat brain L-glutamate transporter. Nature, 360, 464 467.
44. Pippig, S., Andexinger, S. Lohse, M.J. (1995) Sequestration and recycling of beta 2-adrenergic receptors permit receptor resensitization. Mol. Pharmacol., 47, 666 676.
45. Poitry-Yamate, C.L., Vutskits, L. Rauen, T. (2002) Neuronal-induced and glutamate-dependent activation of glial glutamate transporter function. J. Neurochem., 82, 987 997.
46. Pressman, B.C. (1976) Biological applications of ionophores. Annu. Rev. Biochem., 45, 501 530.
47. Qian, Y., Galli, A., Ramamoorthy, S., Risso, S., DeFelice, L.J. Blakely, R.D. (1997) Protein kinase C activation regulates human serotonin transporters in HEK-293 cells via altered cell surface expression. J. Neurosci., 17, 45 57.
48. Ramamoorthy, S. Blakely, R.D. (1999) Phosphorylation and sequestration of serotonin transporters differentially modulated by psychostimulants. Science, 285, 763 766.
49. Robinson, M.B. (2006) Acute regulation of sodium-dependent glutamate transporters: a focus on constitutive and regulated trafficking. Handb. Exp. Pharmacol., 175, 251 275.
50. + channels in spinal cord astrocytes. J. Neurophysiol., 78, 3249 3258.
51. Rothstein, J.D., Dykes-Hoberg, M., Pardo, C.A., Bristol, L.A., Jin, L., Kuncl, R.W., Kanai, Y., Hediger, M.A., Wang, Y., Schielke, J.P. Welty, D.F. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitatory and clearance of glutamate. Neuron, 16, 675 686.
52. Saunders, C., Ferrer, J.V., Shi, L., Chen, J., Merrill, G., Lamb, M.E., Leeb-Lundberg, L.M., Carvelli, L., Javitch, J.A. Galli, A. (2000) Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism. Proc. Natl Acad. Sci. U.S.A., 97, 6850 6855.
53. +-dependent glutamate transporters by cyclic AMP analogs and neurons. Mol. Pharmacol., 53, 355 369.
54. Shigeri, Y., Seal, R.P. Shimamoto, K. (2004) Molecular pharmacology of glutamate transporters, EAATs and VGLUTs. Brain Res. Rev., 45, 250 265.
55. Shimamoto, K., Sakai, R., Takaoka, K., Yumoto, N., Nakajima, T., Amara, S.G. Shigeri, Y. (2004) Characterization of novel L-threo-beta- benzyloxyaspartate derivatives, potent blockers of the glutamate transporters. Mol. Pharmacol., 65, 1008 1015.
56. Shin, H.W., Morinaga, N., Noda, M. Nakayama, K. (2004) BIG2, a guanine nucleotide exchange factor for ADP-ribosylation factors: its localization to recycling endosomes and implication in the endosome integrity. Mol. Biol. Cell, 15, 5283 5294.
57. Sorkina, T., Hoover, B.R., Zahniser, N.R. Sorkin, A. (2005) Constitutive and protein kinase C-induced internalization of the dopamine transporter is mediated by a clathrin-dependent mechanism. Traffic, 6, 157 170.
58. Strous, G.J. Lodish, H.F. (1980) Intracellular transport of secretory and membrane proteins in hepatoma cells infected by vesicular stomatitis virus. Cell, 22, 709 717.
59. Swanson, R.A., Liu, J., Miller, J.W., Rothstein, J.D., Farrell, K., Stein, B.A. Longuemare, M.C. (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J. Neurosci., 17, 932 940.
60. 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. Wada, K. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science, 276, 1699 1702.
61. Tilney, L.G., Connelly, P.S. Portnoy, D.A. (1990) Actin filament nucleation by the bacterial pathogen, Listeria monocytogenes. J. Cell Biol., 111, 2979 2988.
62. Torgersen, M.L., Skretting, G., van Deurs, B. Sandvig, K. (2001) Internalization of cholera toxin by different endocytic mechanisms. J. Cell Sci., 114, 3737 3747.
63. Vanoni, C., Massari, S., Losa, M., Carrega, P., Perego, C., Conforti, L. Pietrini, G. (2004) Increased internalisation and degradation of GLT-1 glial glutamate transporter in a cell model for familial amyotrophic lateral sclerosis (ALS). J. Cell Sci., 117, 5417 5426.
64. Vermeiren, C., Najimi, M., Vanhoutte, N., Tilleux, S., de Hemptinne, I., Maloteaux, J.M. Hermans, E. (2005) Acute up-regulation of glutamate uptake mediated by mGluR5a in reactive astrocytes. J. Neurochem., 94, 405 416.
65. Yu, Y.X., Shen, L., Xia, P., Tang, Y.W., Bao, L. Pei, G. (2006) Syntaxin 1A promotes the endocytic sorting of EAAC1 leading to inhibition of glutamate transport. J. Cell Sci., 119, 3776 3787.
66. Zhou, J. Sutherland, M.L. (2004) Glutamate transporter cluster formation in astrocytic processes regulates glutamate uptake activity. J. Neurosci., 24, 6301 6306.
67. Zschocke, J., Bayatti, N. Behl, C. (2005) Caveolin and GLT-1 gene expression is reciprocally regulated in primary astrocytes: association of GLT-1 with non-caveolar lipid rafts. Glia, 49, 275 287.