Hippocampal glutamate transporter 1 (GLT-1) complex levels are paralleling memory training in the Multiple T-Maze in C57BL/6J mice

Brain Structure and Function

Volumn 217, Issue 2, 2012, Pages 363-378

  Heo, Seok ^a   Jung, Gangsoo ^a   Beuk, Tamara ^a   Höger, Harald ^b   Lubec, Gert ^a  

^a UNIV KLIN KINDER JUGENDHEILKUNDE   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Excitatory amino acid transporter 2; Gel based proteomics; Multidimensional gel electrophoresis; Spatial memory

Indexed keywords

MEMBRANE PROTEIN; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; CONTROLLED STUDY; GLYCOSYLATION; HIPPOCAMPUS; HYDROPHOBICITY; MAZE TEST; MEMORY CONSOLIDATION; MOUSE; MULTIPLE T MAZE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPATIAL MEMORY; TASK PERFORMANCE; TRAINING;

ANIMALS; EXCITATORY AMINO ACID TRANSPORTER 2; GLYCOSYLATION; HIPPOCAMPUS; MALE; MASS SPECTROMETRY; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MODELS, ANIMAL;

ANIMALIA; MUS;

EID: 84862862697     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-011-0362-5     Document Type: Article

References (85)

1. Agnati LF, Ferre S, Burioni R, Woods A, Genedani S, Franco R, Fuxe K (2005) Existence and theoretical aspects of homomeric and heteromeric dopamine receptor complexes and their relevance for neurological diseases. Neuromolecular Med 7:61-78
2. Amara SG, Fontana AC (2002) Excitatory amino acid transporters: keeping up with glutamate. Neurochem Int 41:313-318
3. Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32:1-14
4. Arriza JL, Fairman WA, Wadiche JI, Murdoch GH, Kavanaugh MP, Amara SG (1994) Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J Neurosci 14:5559-5569
5. Autry AE, Grillo CA, Piroli GG, Rothstein JD, McEwen BS, Reagan LP (2006) Glucocorticoid regulation of GLT-1 glutamate transporter isoform expression in the rat hippocampus. Neuroendocrinology 83:371-379
6. Ballif BA, Carey GR, Sunyaev SR, Gygi SP (2008) Large-scale identification and evolution indexing of tyrosine phosphorylation sites from murine brain. J Proteome Res 7:311-318
7. Baucum AJ 2nd, Rau KS, Riddle EL, Hanson GR, Fleckenstein AE (2004) Methamphetamine increases dopamine transporter higher molecular weight complex formation via a dopamine-and hyperthermia-associated mechanism. J Neurosci 24:3436-3443
8. Bauman AL, Apparsundaram S, Ramamoorthy S, Wadzinski BE, Vaughan RA, Blakely RD (2000) Cocaine and antidepressantsensitive biogenic amine transporters exist in regulated complexes with protein phosphatase 2A. J Neurosci 20:7571-7578
9. Bechtholt-Gompf AJ, Walther HV, Adams MA, Carlezon WA Jr, Ongur D, Cohen BM (2010) Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory. Neuropsychopharmacology 35:2049-2059
10. Brooks-Kayal AR, Munir M, Jin H, Robinson MB (1998) The glutamate transporter, GLT-1, is expressed in cultured hippocampal neurons. Neurochem Int 33:95-100
11. Campbell SL, Hablitz JJ (2004) Glutamate transporters regulate excitability in local networks in rat neocortex. Neuroscience 127:625-635
12. Chu K, Lee ST, Sinn DI, Ko SY, Kim EH, Kim JM, Kim SJ, Park DK, Jung KH, Song EC, Lee SK, Kim M, Roh JK (2007) Pharmacological induction of ischemic tolerance by glutamate transporter-1 (EAAT2) upregulation. Stroke 38:177-182
13. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1-105
14. Domercq M, Etxebarria E, Perez-Samartin A, Matute C (2005) Excitotoxic oligodendrocyte death and axonal damage induced by glutamate transporter inhibition. Glia 52:36-46
15. Dunlop J, Lou Z, McIlvain HB (1999a) Steroid hormone-inducible expression of the GLT-1 subtype of high-affinity l-glutamate transporter in human embryonic kidney cells. Biochem Biophys Res Commun 265:101-105
16. Dunlop J, Lou Z, Zhang Y, McIlvain HB (1999b) Inducible expression and pharmacology of the human excitatory amino acid transporter 2 subtype of L-glutamate transporter. Br J Pharmacol 128:1485-1490
17. Fattorini G, Melone M, Bragina L, Candiracci C, Cozzi A, Pellegrini Giampietro DE, Torres-Ramos M, Perez-Samartin A, Matute C, Conti F (2008) GLT-1 expression and Glu uptake in rat cerebral cortex are increased by phencyclidine. Glia 56:1320-1327
18. Furuta A, Rothstein JD, Martin LJ (1997) Glutamate transporter protein subtypes are expressed differentially during rat CNS development. J Neurosci 17:8363-8375
19. Gebhardt FM, Mitrovic AD, Gilbert DF, Vandenberg RJ, Lynch JW, Dodd PR (2010) Exon-skipping splice variants of excitatory amino acid transporter-2 (EAAT2) form heteromeric complexes with full-length EAAT2. J Biol Chem 285:31313-31324
20. Gendreau S, Voswinkel S, Torres-Salazar D, Lang N, Heidtmann H, Detro-Dassen S, Schmalzing G, Hidalgo P, Fahlke C (2004) A trimeric quaternary structure is conserved in bacterial and human glutamate transporters. J Biol Chem 279:39505-39512
21. Genedani S, Guidolin D, Leo G, Filaferro M, Torvinen M, Woods AS, Fuxe K, Ferre S, Agnati LF (2005) Computer-assisted image analysis of caveolin-1 involvement in the internalization process of adenosine A2A-dopamine D2 receptor heterodimers. J Mol Neurosci 26:177-184
22. Ghafari M, Falsafi SK, Hoeger H, Lubec G (2011) Hippocampal levels of GluR1 and GluR2 complexes are modulated by training in the Multiple T-Maze in C57BL/6J mice. Brain Struct Funct (in press), doi:10.1007/s00429-011-0335-8
23. Gonzalez MI, Robinson MB(2004) Neurotransmitter transporters: why dance with so many partners? Curr Opin Pharmacol 4:30-35
24. Gonzalez MI, Susarla BT, Robinson MB (2005) Evidence that protein kinase Calpha interacts with and regulates the glial glutamate transporter GLT-1. J Neurochem 94:1180-1188
25. Gonzalez-Gonzalez IM, Garcia-Tardon N, Gimenez C, Zafra F (2009) Splice variants of the glutamate transporter GLT1 form hetero-oligomers that interact with PSD-95 and NMDA receptors. J Neurochem 110:264-274
26. Hadlock GC, Baucum AJ II, King JL, Horner KA, Cook GA, Gibb JW, Wilkins DG, Hanson GR, Fleckenstein AE (2009) Mechanisms underlying methamphetamine- induced dopamine transporter complex formation. J Pharmacol Exp Ther 329:169-174
27. Hadlock GC, Chu PW, Walters ET, Hanson GR, Fleckenstein AE (2010) Methamphetamine-induced dopamine transporter complex formation and dopaminergic deficits: the role of D2 receptor activation. J Pharmacol Exp Ther 335:207-212
28. Haugeto O, Ullensvang K, Levy LM, Chaudhry FA, Honore T, Nielsen M, Lehre KP, Danbolt NC (1996) Brain glutamate transporter proteins form homomultimers. J Biol Chem 271:27715-27722
29. Hediger MA, Kanai Y, You G, Nussberger S (1995) Mammalian ioncoupled solute transporters. J Physiol 482:7S-17S
30. Heo S, Lubec G (2010) Generation and characterization of a specific polyclonal antibody against the mouse serotonin receptor 1A: a state-of-the-art recommendation on how to characterize antibody specificity. Electrophoresis 31:3789-3796
31. Heo S, Kang SU, Oehler R, Pollak A, Lubec G (2010) Mass spectrometrical analysis of the mitochondrial carrier Aralar1 from mouse hippocampus. Electrophoresis 31:1813-1821
32. Hinoi E, Takarada T, Tsuchihashi Y, Yoneda Y (2005) Glutamate transporters as drug targets. Curr Drug Targets CNS Neurol Disord 4:211-220
33. Huang YH, Sinha SR, Tanaka K, Rothstein JD, Bergles DE (2004) Astrocyte glutamate transporters regulate metabotropic glutamate receptor-mediated excitation of hippocampal interneurons. J Neurosci 24:4551-4559
34. Kanai Y, Hediger MA (2004) The glutamate/neutral amino acid transporter family SLC1: molecular, physiological and pharmacological aspects. Pflugers Arch 447:469-479
35. Kang SU, Lubec G (2009) Complete sequencing of GABAA receptor subunit beta 3 by a rapid technique following in-gel digestion of the protein. Electrophoresis 30:2159-2167
36. Kang SU, Fuchs K, Sieghart W, Lubec G (2008) Gel-based mass spectrometric analysis of recombinant GABA(A) receptor subunits representing strongly hydrophobic transmembrane proteins. J Proteome Res 7:3498-3506
37. Kang SU, Fuchs K, Sieghart W, Pollak A, Csaszar E, Lubec G (2009) Gel-based mass spectrometric analysis of a strongly hydrophobic GABAA-receptor subunit containing four transmembrane domains. Nat Protoc 4:1093-1102
38. Kang SU, Heo S, Lubec G (2011) Mass spectrometric analysis of GABA(A) receptor subtypes and phosphorylations from mouse hippocampus. Proteomics 11:2171-2181
39. Katagiri H, Tanaka K, Manabe T (2001) Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 14:547-553
40. Kirschner MA, Copeland NG, Gilbert DJ, Jenkins NA, Amara SG (1994) Mouse excitatory amino acid transporter EAAT2: isolation, characterization, and proximity to neuroexcitability loci on mouse chromosome 2. Genomics 24:218-224
41. Lee Y, Gaskins D, Anand A, Shekhar A (2007) Glia mechanisms in mood regulation: a novel model of mood disorders. Psychopharmacology (Berl) 191:55-65
42. Li LB, Toan SV, Zelenaia O, Watson DJ, Wolfe JH, Rothstein JD, Robinson MB (2006) Regulation of astrocytic glutamate transporter expression by Akt: evidence for a selective transcriptional effect on the GLT-1/EAAT2 subtype. J Neurochem 97:759-771
43. Lomberk G, Bensi D, Fernandez-Zapico ME, Urrutia R (2006) Evidence for the existence of an HP1-mediated subcode within the histone code. Nat Cell Biol 8:407-415
44. Maragakis NJ, Dykes-Hoberg M, Rothstein JD (2004) Altered expression of the glutamate transporter EAAT2b in neurological disease. Ann Neurol 55:469-477
45. Matute C, Melone M, Vallejo-Illarramendi A, Conti F (2005) Increased expression of the astrocytic glutamate transporter GLT-1 in the prefrontal cortex of schizophrenics. Glia 49:451-455
46. McCullumsmith RE, Meador-Woodruff JH (2002) Striatal excitatory amino acid transporter transcript expression in schizophrenia, bipolar disorder, and major depressive disorder. Neuropsychopharmacology 26:368-375
47. Mennerick S, Dhond RP, Benz A, Xu W, Rothstein JD, Danbolt NC, Isenberg KE, Zorumski CF (1998) Neuronal expression of the glutamate transporter GLT-1 in hippocampal microcultures. J Neurosci 18:4490-4499
48. Meyer T, Ludolph AC, Morkel M, Hagemeier C, Speer A (1997) Genomic organization of the human excitatory amino acid transporter gene GLT-1. Neuroreport 8:775-777
49. Meyer T, Munch C, Liebau S, Fromm A, Schwalenstocker B, Volkel H, Ludolph AC (1998) Splicing of the glutamate transporter EAAT2: a candidate gene of amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry 65:954
50. Mukainaka Y, Tanaka K, Hagiwara T, Wada K (1995) Molecular cloning of two glutamate transporter subtypes from mouse brain. Biochim Biophys Acta 1244:233-237
51. Munir M, Correale DM, Robinson MB (2000) Substrate-induced upregulation of Na(?)-dependent glutamate transport activity. Neurochem Int 37:147-162
52. Munton RP, Tweedie-Cullen R, Livingstone-Zatchej M, Weinandy F, Waidelich M, Longo D, Gehrig P, Potthast F, Rutishauser D, Gerrits B, Panse C, Schlapbach R, Mansuy IM (2007) Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol Cell Proteomics 6:283-293
53. Nuwal T, Heo S, Lubec G, Buchner E (2011) Mass spectrometric analysis of synapsins in Drosophila melanogaster and identification of novel phosphorylation sites. J Proteome Res 10:541-550
54. Ohnuma T, Tessler S, Arai H, Faull RL, McKenna PJ, Emson PC (2000) Gene expression of metabotropic glutamate receptor 5 and excitatory amino acid transporter 2 in the schizophrenic hippocampus. Brain Res Mol Brain Res 85:24-31
55. Omrani A, Melone M, Bellesi M, Safiulina V, Aida T, Tanaka K, Cherubini E, Conti F (2009) Up-regulation of GLT-1 severely impairs LTD at mossy fibre-CA3 synapses. J Physiol 587:4575-4588
56. O'Shea RD (2002) Roles and regulation of glutamate transporters in the central nervous system. Clin Exp Pharmacol Physiol 29:1018-1023
57. Patil SS, Sunyer B, Hoger H, Lubec G (2009) Evaluation of spatial memory of C57BL/6J and CD1 mice in the Barnes maze, the Multiple T-maze and in the Morris water maze. Behav Brain Res 198:58-68
58. Pawlak J, Brito V, Kuppers E, Beyer C (2005) Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Brain Res Mol Brain Res 138:1-7
59. Peacey E, Miller CC, Dunlop J, Rattray M (2009) The four major Nand C-terminal splice variants of the excitatory amino acid transporter GLT-1 form cell surface homomeric and heteromeric assemblies. Mol Pharmacol 75:1062-1073
60. Pei L, Li S, Wang M, Diwan M, Anisman H, Fletcher PJ, Nobrega JN, Liu F (2010) Uncoupling the dopamine D1-D2 receptor complex exerts antidepressant-like effects. Nat Med 16:1393-1395
61. 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
62. Qu S, Kanner BI (2008) Substrates and non-transportable analogues induce structural rearrangements at the extracellular entrance of the glial glutamate transporter GLT-1/EAAT2. J Biol Chem 283:26391-26400
63. Raunser S, Haase W, Bostina M, Parcej DN, Kuhlbrandt W (2005) High-yield expression, reconstitution and structure of the recombinant, fully functional glutamate transporter GLT-1 from Rattus norvegicus. J Mol Biol 351:598-613
64. Regan MR, Huang YH, Kim YS, Dykes-Hoberg MI, Jin L, Watkins AM, Bergles DE, Rothstein JD (2007) 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
65. Robinson MB (1998) The family of sodium-dependent glutamate transporters: a focus on the GLT-1/EAAT2 subtype. Neurochem Int 33:479-491
66. Rose EM, Koo JC, Antflick JE, Ahmed SM, Angers S, Hampson DR (2009) Glutamate transporter coupling to Na, K-ATPase. J Neurosci 29:8143-8155
67. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kuncl RW, Kanai Y, Hediger MA, Wang Y, Schielke JP, Welty DF (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16:675-686
68. Sattler R, Rothstein JD (2006) Regulation and dysregulation of glutamate transporters. Handb Exp Pharmacol 175:277-303
69. Schmitt A, Zink M, Petroianu G, May B, Braus DF, Henn FA (2003) Decreased gene expression of glial and neuronal glutamate transporters after chronic antipsychotic treatment in rat brain. Neurosci Lett 347:81-84
70. Sheldon AL, Robinson MB (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51:333-355
71. Sims KD, Robinson MB (1999) Expression patterns and regulation of glutamate transporters in the developing and adult nervous system. Crit Rev Neurobiol 13:169-197
72. Sitcheran R, Gupta P, Fisher PB, Baldwin AS (2005) Positive and negative regulation of EAAT2 by NF-kappaB: a role for N-myc in TNFalpha-controlled repression. EMBO J 24:510-520
73. Smith RE, Haroutunian V, Davis KL, Meador-Woodruff JH (2001) Expression of excitatory amino acid transporter transcripts in the thalamus of subjects with schizophrenia. Am J Psychiatry 158:1393-1399
74. Suchak SK, Baloyianni NV, Perkinton MS, Williams RJ, Meldrum BS, Rattray M (2003) The 'glial' glutamate transporter, EAAT2 (Glt-1) accounts for high affinity glutamate uptake into adult rodent nerve endings. J Neurochem 84:522-532
75. Sutherland ML, Delaney TA, Noebels JL (1995) Molecular characterization of a high-affinity mouse glutamate transporter. Gene 162:271-274
76. Swamy M, Siegers GM, Minguet S, Wollscheid B, Schamel WW (2006) Blue native polyacrylamide gel electrophoresis (BNPAGE) for the identification and analysis of multiprotein complexes. Sci STKE 2006:pl4
77. Swanson RA, Liu J, Miller JW, Rothstein JD, Farrell K, Stein BA, Longuemare MC (1997) Neuronal regulation of glutamate transporter subtype expression in astrocytes. J Neurosci 17:932-940
78. Takatsuru Y, Iino M, Tanaka K, Ozawa S (2007) Contribution of glutamate transporter GLT-1 to removal of synaptically released glutamate at climbing fiber-Purkinje cell synapses. Neurosci Lett 420:85-89
79. Tanaka K (2000) Functions of glutamate transporters in the brain. Neurosci Res 37:15-19
80. 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
81. Tordera RM, Totterdell S, Wojcik SM, Brose N, Elizalde N, Lasheras B, Del Rio J (2007) Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur J Neurosci 25:281-290
82. Utsunomiya-Tate N, Endou H, Kanai Y (1997) Tissue specific variants of glutamate transporter GLT-1. FEBS Lett 416:312-316
83. Williams SM, Sullivan RK, Scott HL, Finkelstein DI, Colditz PB, Lingwood BE, Dodd PR, Pow DV (2005) Glial glutamate transporter expression patterns in brains from multiple mammalian species. Glia 49:520-541
84. Zerangue N, Kavanaugh MP (1996) Flux coupling in a neuronal glutamate transporter. Nature 383:634-637
85. Zhang H, Xin W, Dougherty PM (2009) Synaptically evoked glutamate transporter currents in Spinal Dorsal Horn Astrocytes. Mol Pain 5:36