Changes in glial glutamate transporters in human epileptogenic hippocampus: Inadequate explanation for high extracellular glutamate during seizures

Neurobiology of Disease

Volumn 25, Issue 2, 2007, Pages 319-330

  Bjornsen L P ^b   Eid, T ^a   Holmseth, S ^b   Danbolt, N C ^b   Spencer, D D ^a   de Lanerolle, N C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Astrocytes; EAAT; GLAST; GLT 1; Glutamate; Hippocampus; MTLE; Temporal lobe epilepsy

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

ADOLESCENT; ADULT; ARTICLE; ASTROCYTE; BRAIN REGION; CELL LOSS; CLINICAL ARTICLE; CONTROLLED STUDY; DIALYSIS; DOWN REGULATION; FEMALE; GLIA; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; NERVE CELL; NERVE CELL LOSS; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCHOOL CHILD; SEIZURE; SUBICULUM; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; ADULT; AMINO ACID TRANSPORT SYSTEM X-AG; ASTROCYTES; CHILD; CHILD, PRESCHOOL; DOWN-REGULATION; EPILEPSY; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; EXTRACELLULAR FLUID; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; UP-REGULATION;

EID: 33846321268     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2006.09.014     Document Type: Article

References (63)

1. Akbar M.T., Rattray M., Williams R.J., Chong N.W.S., and Meldrum B.S. Reduction of GABA and glutamate transporter messenger RNAs in the severe-seizure genetically epilepsy-prone rat. Neuroscience 85 (1998) 1235-1251
2. Amaral D.G., and Insausti R. Hippocampal formation. In: Paxinos G. (Ed). The Human Nervous System (1990), Academic Press, San Diego 711-756
3. Arriza J.L., Eliasof S., Kavanaugh M.P., and Amara S.G. Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 4155-4160
4. Beckstrom H., Julsrud L., Haugeto O., Dewar D., Graham D.I., Lehre K.P., Storm-Mathiesen J., and Danbolt N.C. Interindividual differences in the levels of the glutamate transporters GLAST and GLT, but no clear correlation with Alzheimer's disease. J. Neurosci. Res. 55 (1999) 218-229
5. Broman J., Hassel B., Rinvik E., and Ottersen O.P. Biochemistry and anatomy of transmitter glutamate. In: Ottersen O.P., and Storm-Mathisen J. (Eds). Glutamate vol. 18 (2000), Elsevier Science B.V., Amsterdam 1-44
6. Cavus I., Kasoff W.S., Cassaday M.P., Jacob R., Gueorguieva R., Sherwin R.S., Krystal J., Spencer D.D., and Abi-Saab W. Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann. Neurol. 57 (2005) 226-235
7. Chadwick D. The epidemiology of drug resistant epilepsy and adverse effects of antiepileptic drugs. Acta Neurochir., Suppl. (Wien.) 50 (1990) 32-37
8. Chaudhry F.A., Lehre K.P., van Lookeren Campagne M., Ottersen O.P., Danbolt N.C., and Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15 (1995) 711-720
9. Crino P.B., Jin H., Shumate M.D., Robinson M.B., Coulter D.A., and Brookskayal R. Increased expression of neuronal glutamate transporter (EAAT3/EAAC1) in hippocampal and neocortical epilepsy. Epilepsia 43 (2002) 211-218
10. Danbolt N.C. Glutamate uptake. Prog. Neurobiol. 65 (2001) 1-105
11. +]coupled l-glutamate transporter purified from rat brain is located in glial cell processes. Neuroscience 51 (1992) 295-310
12. Danbolt N.C., Lehre K.P., Dehnes Y., Chaudhry F.A., and Levy L.M. Localization of transporters using transporter-specific antibodies. Methods Enzymol. 296 (1998) 388-407
13. de Lanerolle N.C., and Lee T.S. New facets of the neuropathology and molecular profile of human temporal lobe epilepsy. Epilepsy Behav. 7 (2005) 190-203
14. de Lanerolle N.C., Kim J.H., and Brines M.L. Cellular and molecular alterations in partial epilepsy. Clin. Neurosci. 2 (1994) 64-81
15. de Lanerolle N.C., Eid T., von Campe G., Kovacs I., Spencer D.D., and Brines M.L. Glutamate receptor subunits GluR1 and GluR2/3 distribution shows reorganization in the human epileptogenic hippocampus. Eur. J. Neurosci. 10 (1998) 1687-1703
16. de Lanerolle N.C., Kim J.H., Williamson A., Spencer S.S., Zaveri H.P., Eid T., and Spencer D.D. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44 (2003) 677-687
17. Dehnes Y., Chaudhry F.A., Ullensvang K., Lehre K.P., Storm-Mathiesen J., and Danbolt N.C. 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 (1998) 3606-3619
18. During M.J., and Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341 (1993) 1607-1610
19. Eid T., Thomas M.J., Spencer D.D., Rundén-Pran E., Kim J.H., Ottersen O.P., and de Lanerolle N.C. Loss of glutamine synthetase in the human epileptogenic hippocampus: a possible mechanism for elevated extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363 (2004) 28-37
20. Fairman W.A., Vandenberg R.J., Arizza J.L., Kavanaugh M.P., and Amara S.G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375 (1995) 599-603
21. Ferrie C.D., Bird S., Tilling K., Maisey M.N., Chapman A.G., and Robinson R.O. Plasma amino acids in childhood epileptic encephalopathies. Epilepsy Res. 34 (1999) 221-229
22. Ghijsen W.E.J.M., Belo A.I.D.A., Zuiderwijk M., and da Silva F.H.L. Compensatory changes in EAAC1 glutamate transporter in rat hippocampus CA1 region during kindling epileptogenesis. Neurosci. Lett. 276 (1999) 157-160
23. Gorter J.A., Van Vliet E.A., Proper E.A., De Graan P.N.E., Ghijsen W.E.J.M., da Silva F.H.L., and Aronica E. Glutamate transporter alterations in the reorganizing dentate gyrus are associated with progressive seizure activity in chronic epileptic rats. J. Comp. Neurol. 442 (2002) 365-377
24. Haugeto Ø., Ullensvang K., Levy L.M., Chaudhry F.A., Honore T., Nielsen M., Lehre K.P., and Danbolt N.C. Brain glutamate transporter proteins form homomultimers. J. Biol. Chem. 271 (1996) 27715-27722
25. Hauser W.A., and Kurland L.T. The epidemiology of epilepsy in Rochester, Minnesota 1935 through 1967. Epilepsia 16 (1975) 1-66
26. Hoogland G., van Oort R.J., Proper E.A., Jansen G.H., van Rijen P.C., van Veelen C.W.M., van Nieuwenhuizen O., Troost D., and de Graan P.N.E. Alternative splicing of glutamate transporter EAAT2 RNA in neocortex and hippocampus of temporal lobe epilepsy patients. Epilepsy Res. 59 (2004) 75-82
27. Hsu S., Raine L., and Fanger H. The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29 (1981) 577-580
28. Ingram E.M., Wiseman J.W., Tessler S., and Emson P.C. Reduction of glial glutamate transporters in the parietal cortex and hippocampus of the EL mouse. J. Neurochem. 79 (2001) 564-575
29. Janjua N.A., Itano T., Kugoh T., Hosokawa K., Nakano M., Matsui H., and Hatase O. Familial increase in plasma glutamic acid in epilepsy. Epilepsy Res. 11 (1992) 37-44
30. Kanai Y., and Hediger M.A. Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360 (1992) 467-471
31. Kim J.H. Pathology of epilepsy. Exp. Mol. Pathol. 70 (2001) 345-367
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 360 (1970) 467-471
33. Lehre K.P., Levy L.M., Ottersen O.P., Storm-Mathisen J., and Danbolt N.C. Differential expression of two glial glutamate transporters in the rat brain: quantitative and immunocytochemical observations. J. Neurosci. 15 (1995) 1835-1853
34. +]coupled l-glutamate transporter purified from rat brain confirms glial cell localization. FEBS Lett. 317 (1993) 79-84
35. Lorente de Nó R. Studies on the structure of the cerebral cortex. II: Continuation of the study of the ammonic system. J. Psychol. Neurol. (Leipzig) 46 (1934) 113-177
36. Mathern G.W., Babb T.L., and Armstrong D.L. Hippocampal sclerosis. In: Engel J., and Pedley T.A. (Eds). Epilepsy: A Comprehensive Textbook (1997), Lippincott-Raven, Philadelphia 133-155
37. Mathern G.W., Mendoza D., Lozada A., Pretorius J.K., Dehnes Y., Danbolt N.C., Nelson N., Leite J.P., Chimelli L., Born D.E., Sakamoto A.C., Assirati J.A., Fried I., Peacock W.J., Ojemann G.A., and Adelson P.D. Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52 (1999) 453-472
38. Meldrum B.S. The role of glutamate in epilepsy and other CNS disorders. Neurology 44 (1994) 14-23
39. Meldrum B.S., Akbar M.T., and Chapman A.G. Glutamate receptors and transporters in genetic and acquired models of epilepsy. Epilepsy Res. 36 (1999) 189-204
40. Milton I.D., Banner S.J., Ince P.G., Piggott N.H., Fray A.E., Thatcher N., Horne C.H.W., and Shaw P.J. Expression of glial glutamate transporter EAAT2 in the human CNS: an immunohistochemical study. Mol. Brain Res. 52 (1997) 17-31
41. Musshoff U., Schünke U., Köhling R., and Speckmann E.J. Alternative splicing of the NMDAR1 glutamate receptor subunit in human temporal lobe epilepsy. Mol. Brain Res. 76 (2000) 377-384
42. Nagao S., Kwak S., and Kanazawa I. EAAT4, a glutamate transporter with properties of a chloride channel, is predominantly localized in Purkinje cell dendrites, and forms parasagittal compartments in rat cerebellum. Neuroscience 78 (1997) 929-933
43. Nonaka M., Kohmura E., Yamashita T., Shimada S., Tanaka K., Yoshimine T., Tohyama M., and Hayakawa T. Increased transcription of glutamate-aspartate transporter (GLAST/GluT-1) mRNA following kainic acid-induced limbic seizure. Brain Res. Mol. Brain Res. 55 (1998) 54-60
44. Olney J.W. Neurotoxicity of excitatory amino acids. In: McGeer E.G., Olney J.W., and McGeer P.L. (Eds). Kainic Acid as a Tool in Neurobiology (1978), Raven Press, New York 37-70
45. Olney J.W., Collins R.C., and Sloviter R.S. Excitotoxic mechanisms of epileptic brain damage. In: Delgado-Escueta A.V., Ward Jr. A.A., Woodbury D.M., and Porter R.J. (Eds). Advances in Neurology (1986), Raven Press, New York 857-877
46. Peghini P., Janzen J., and Stoffel W. Glutamate transporter EAAX-1-deficient mice develop dicarboxylic aminoaciduria and behavioral abnormalities but no neurodegeneration. The EMBO J. 16 (1997) 3822-3832
47. Pines G., Danbolt N.C., Bjørås M., Zhang Y., Bendahan A., Eide L., Koepsell H., Storm-Mathiesen J., Seeberg E., and Kanner B.I. Cloning and expression of a rat brain l-glutamate transporter. Nature 360 (1992) 464-467
48. Proper E.A., Hoogland G., Kappen S.M., Jansen G.H., Rensen M.G.A., Schrama L.H., van Veelen C.W.M., van Rijen P.C., van Nieuwenhuizen O., Gipsen W.H., and de Graan P.N.E. Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125 (2002) 32-43
49. Rothstein J.D., Martin L., Levey A.I., Dykes-Hogberg M., Jin L., Wu D., Nash N., and Kuncl R.W. Localization of neuronal and glial glutamate transporters. Neuron 13 (1994) 713-725
50. Samuelsson C., Kumlien E., Flink R., Lindholm D., and Ronne-Engstrom E. Decreased cortical levels of astrocytic glutamate transport protein GLT-1 in a rat model of posttraumatic epilepsy. Neurosci. Lett. 289 (2000) 185-188
51. Simantov R., Crispino M., Hoe W., Broutman G., Tocco G., Rothstein J.D., and Baudry M. Changes in expression of neuronal and glial glutamate transporters in rat hippocampus following kainate-induced seizure activity. Brain Res. Mol. Brain Res. 65 (1999) 112-123
52. Sommer W. Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch. Psychiatr. Nervenkr. 10 (1880) 631-675
53. Spencer D.D., and Inserni J. Temporal lobectomy. In: Lüders H.O. (Ed). Epilepsy Surgery (1991), Raven Press, Ltd., New York 533-545
54. Spencer D.D., Spencer S.S., Mattson R.H., Williamson P.D., and Novelly R. Access to posterior medial temporal lobe structures in the surgical treatment of temporal lobe epilepsy. Neurosurgery 15 (1984) 667-671
55. Storck T., Schulte S., Hofmann K., and Stoffel W. Structure, expression, and functional analysis of a Na+-dependent glutamate/aspartate transporter from rat brain. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 10955-10959
56. Tanaka K. Cloning and expression of a glutamate transporter from mouse brain. Neurosci. Lett. 159 (1993) 183-186
57. Tanaka K., Watase K., Manabe T., Yamada K., Watanabe M., Takahashi K., Iwama H., Nishikawa T., Ichihara N., Hori S., Takimoto M., and Wada K. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276 (1997) 1699-1702
58. Tessler S., Danbolt N.C., Faull R.L.M., Storm-Mathisen J., and Emson P. Expression of the glutamate transporters in human temporal lobe epilepsy. Neuroscience 88 (1998) 1083-1091
59. Tian G.-F., Azmi H., Takano T., Xu Q., Peng W., Lin J., Oberheim N., Lou N., Wang X., Zielke H.R., Kang J., and Nedergaard M. An astrocytic basis of epilepsy. Nat. Med. 11 (2005) 973-981
60. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacremalide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 4350-4354
61. Ueda Y., Doi T., Tokumaru J.H.Y., Nakajima A., Mitsuyama Y., Ohyanishiguchi H., Kamada H., and Willmore L.J. Collapse of extracellular glutamate regulation during epileptogenesis: down-regulation and functional failure of glutamate transporter function in rats with chronic seizures induced by kainic acid. J. Neurochem. 76 (2001) 892-900
62. Williamson A. Electrophysiology of epileptic human neocortical and hippocampal neurons maintained in vitro. Clin. Neurosci. 2 (1994) 47-52
63. Yamada K., Watanabe M., Shibata T., Tanaka K., Wada K., and Inoue Y. EAAT4 is a post-synaptic glutamate transporter at Purkinje cell synapses. NeuroReport 7 (1996) 2013-2017