Loss of glutamine synthetase in the human epileptogenic hippocampus: Possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy

Lancet

Volumn 363, Issue 9402, 2004, Pages 28-37

  Eid, T ^a   Thomas, M J ^b   Spencer, D D ^a   Runden Pran E ^b   Lai, J C K ^c   Malthankar, G V ^c   Kim, J H ^a   Danbolt, N C ^b   Ottersen, O P ^b   De Lanerolle, N C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

^c IDAHO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE AMMONIA LIGASE; GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

ADOLESCENT; ADULT; ARTICLE; ASTROCYTE; CATABOLISM; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME DEFICIENCY; ENZYME LOCALIZATION; EPILEPTOGENESIS; EXTRACELLULAR SPACE; FEMALE; HIPPOCAMPUS; HOMEOSTASIS; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MACROGLIA; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; SAMPLING; SCHOOL CHILD; SEIZURE; STANDARDIZATION; STATISTICAL SIGNIFICANCE; SURGICAL TECHNIQUE; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING;

EID: 9144228368     PISSN: 01406736     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0140-6736(03)15166-5     Document Type: Article

References (44)

1. Theodore W. What is uncontrolled epilepsy, and who should be referred for surgery? Spencer S.S., Spencer D.D. Surgery for epilepsy. 1991;3-17 Blackwell, Boston.
2. Spencer D.D., Spencer S.S., Mattson R.H., Williamson P.D., Novelly R. Access to the posterior medial temporal lobe structures in the surgical treatment of temporal lobe epilepsy. Neurosurgery. 15:1984;667-671.
3. de Lanerolle N.C., Kim J.H., Brines M.L. Cellular and molecular alterations in partial epilepsy. Clin Neurosci. 2:1994;64-81.
4. Sommer W. Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch Psychiatr Nervenkr. 10:1880;631-675.
5. Spencer D.D. Classifying the epilepsies by substrate. Clin Neurosci. 2:1994;104-109.
6. de Lanerolle N.C., Kim J.H., Williamson A., et al. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia. 44:2003;677-687.
7. Mathern G.W., Babb T.L., Armstrong D.L. Hippocampal sclerosis. Engel J., Pedley T.A. Epilepsy: a comprehensive textbook. 1997;133-155 Lippincott-Raven, Philadelphia.
8. During M.J., Spencer D.D. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet. 341:1993;1607-1610.
9. Olney J.W. Neurotoxicity of excitatory amino acids. McGeer E.G., Olney J.W., McGeer P.L. Kainic acid as a tool in neurobiology. 1978;37-70 Raven Press, New York.
10. Olney J.W., Collins R.C., Sloviter R.S. Excitotoxic mechanims of epileptic brain damage. Delgado-Escueta A.V., Ward AA Jr, Woodbury D.M., Porter R.J. Advances in neurology. 1986;857-877 Raven Press, New York.
11. Williamson A. Electrophysiology of epileptic human neocortical and hippocampal neurons maintained in vitro. Clin Neurosci. 2:1994;47-52.
12. de Lanerolle N.C., Eid T., von Campe G., Kovacs I., Spencer D.D., Brines M. Glutamate receptor subunits GluR1 and GluR2/3 distribution shows reorganization in the human epileptogenic hippocampus. Eur J Neurosci. 10:1998;1687-1703.
13. Broman J., Hassel B., Rinvik E., Ottersen O.P. Biochemistry and anatomy of transmitter glutamate. Ottersen O.P., Storm-Mathisen J. Glutamate. 2000;1-44 Elsevier Science, Amsterdam.
14. Eisenberg D., Gill H.S., Pfluegl G.M., Rotstein S.H. Structure-function relationships of glutamine synthetases. Biochim Biophys Acta. 1477:2000;122-145.
15. van den Berg C.J., Garfinkel D. A stimulation study of brain compartments: metabolism of glutamate and related substances in mouse brain. Biochem J. 123:1971;211-218.
16. Petroff O.A., Errante L.D., Rothman D.L., Kim J.H., Spencer D.D. Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia. 43:2002;703-710.
17. Eid T, Thomas MJ, Spencer DD, Ottersen OP, de Lanerolle NC. Downregulation of glutamine synthetase in the human epileptogenic hippocampus despite glial proliferation: a key to sustained levels of glutamate during seizures? Epilepsia 2002; 43 (suppl): 3.039.
18. 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.
19. Kim J.H. Pathology of epilepsy. Exp Mol Pathol. 70:2001;345-367.
20. Danbolt N.C., Lehre K.P., Dehnes Y., Chaudhry F.A., Levy L.M. Localization of transporters using transporter-specific antibodies. Methods Enzymol. 296:1998;388-407.
21. Beckstrom H., Julsrud L., Haugeto O., et al. 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.
22. Hsu S., Raine L., 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.
23. Dennis S.C., Lai J.C., Clark J.B. The distribution of glutamine synthetase in subcellular fractions of rat brain. Brain Res. 197:1980;469-475.
24. Danbolt N.C. Glutamate uptake. Prog Neurobiol. 65:2001;1-105.
25. Otis T.S., Jahr C.E. Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci. 18:1998;7099-7110.
26. Meister A. Inhibition of glutamine synthetase and gamma-glutamylcysteine synthetase by methionine sulfoximine and related compounds. Seiler N., Jung M., Koch-Weser J. Enzyme activated irreversible inhibitors. 1978;187-210 Elsevier, Amsterdam.
27. Laake J.H., Slyngstad T.A., Haug F.M., Ottersen O.P. Glutamine from glial cells is essential for the maintenance of the nerve terminal pool of glutamate: immunogold evidence from hippocampal slice cultures. J Neurochem. 65:1995;871-881.
28. Shaw C.A., Bains J.S., Pasqualotto B.A., Curry K. Methionine sulfoximine shows excitotoxic actions in rat cortical slices. Can J Physiol Pharmacol. 77:1999;871-877.
29. Shaked I., Ben-Dror I., Vardimon L. Glutamine synthetase enhances the clearance of extracellular glutamate by the neural retina. J Neurochem. 83:2002;574-580.
30. Gorovits R., Avidan N., Avisar N., Shaked I., Vardimon L. Glutamine synthetase protects against neuronal degeneration in injured retinal tissue. Proc Natl Acad Sci USA. 94:1997;7024-7029.
31. Szegedy L. Enzyme histochemical studies in the rat hippocampus, cerebellar cortex and brainstem motor nuclei during methionine sulphoximine convulsions. Cell Mol Biol. 23:1978;43-53.
32. Folbergrova J., Passonneau J.V., Lowry O.H., Schulz D.W. Glycogen, ammonia and related metabolites in the brain during seizures evoked by methionine sulphoximine. J Neurochem. 16:1969;191-203.
33. Laming P.R., Cosby S.L., O'Neill J.K. Seizures in the Mongolian gerbil are related to a deficiency in cerebral glutamine synthetase. Comp Biochem Physiol C. 94:1989;399-404.
34. Walz W., Lang M.K. Immunocytochemical evidence for a distinct GFAP-negative subpopulation of astrocytes in the adult rat hippocampus. Neurosci Lett. 257:1998;127-130.
35. Condorelli D.F., Dell'Albani P., Kaczmarek L., et al. Glial fibrillary acidic protein messenger RNA and glutamine synthetase activity after nervous system injury. J Neurosci Res. 26:1990;251-257.
36. Blondet B., Hantaz-Ambroise D., Ait-Ikhlef A., Cambier D., Murawsky M., Rieger F. Astrocytosis in wobbler mouse spinal cord involves a population of astrocytes which is glutamine synthetase-negative. Neurosci Lett. 183:1995;179-182.
37. Derouiche A., Heimrich B., Frotscher M. Loss of layer-specific astrocytic glutamine synthetase immunoreactivity in slice cultures of hippocampus. Eur J Neurosci. 5:1993;122-127.
38. Jackson M.J., Zielke H.R., Max S.R. Effect of dibutyryl cyclic AMP and dexamethasone on glutamine synthetase gene expression in rat astrocytes in culture. Neurochem Res. 20:1995;201-207.
39. Stanimirovic D.B., Ball R., Small D.L., Muruganandam A. Developmental regulation of glutamate transporters and glutamine synthetase activity in astrocyte cultures differentiated in vitro. Int J Dev Neurosci. 17:1999;173-184.
40. Vardimon L., Ben-Dror I., Avisar N., Oren A., Shiftan L. Glucocorticoid control of glial gene expression. J Neurobiol. 40:1999;513-527.
41. Beer J., Mielke K., Zipp M., Zimmermann M., Herdegen T. Expression of c-jun, junB, c-fos, fra-1 and fra-2 mRNA in the rat brain following seizure activity and axotomy. Brain Res. 794:1998;255-266.
42. Huang T.L., O'Banion M.K. Interleukin-1 beta and tumor necrosis factor-alpha suppress dexamethasone induction of glutamine synthetase in primary mouse astrocytes. J Neurochem. 71:1998;1436-1442.
43. Kruchkova Y., Ben-Dror I., Herschkovitz A., David M., Yayon A., Vardimon L. Basic fibroblast growth factor: a potential inhibitor of glutamine synthetase expression in injured neural tissue. J Neurochem. 77:2001;1641-1649.
44. Liu Z., Holmes G.L. Basic fibroblast growth factor-induced seizures in rats. Neurosci Lett. 233:1997;85-88.