Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats

Brain

Volumn 131, Issue 8, 2008, Pages 2061-2070

  Eid, Tore ^a   Ghosh, Arko ^a   Wang, Yue ^a   Beckström, Henning ^a,b   Zaveri, Hitten P ^a   Lee, Tih Shih W ^a   Lai, James C K ^c   Malthankar Phatak, Gauri H ^c   De Lanerolle, Nihal C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

^c IDAHO STATE UNIVERSITY   (United States)

Author keywords

Animal models; Astrocyte; Epileptiform EEG discharges; Glutamate; Temporal lobes

Indexed keywords

GLUTAMATE AMMONIA LIGASE; METHIONINE SULFOXIMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME INHIBITION; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; MALE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; RECURRENT DISEASE; SEIZURE; TEMPORAL LOBE EPILEPSY;

ANIMALS; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; GLUTAMATE-AMMONIA LIGASE; GLUTATHIONE; HIPPOCAMPUS; MALE; METHIONINE SULFOXIMINE; MODELS, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY; RECURRENCE;

EID: 49449111897     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn133     Document Type: Article

References (45)

1. Adams ME, Kramarcy N, Krall SP, Rossi SG, Rotundo RL, Sealock R, et al. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J Cell Biol 2000; 150: 1385-98.
2. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, et al. Delayed K+ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci USA 2003; 100: 13615-20.
3. Babb TL, Brown WJ, Pretorius J, Davenport C, Lieb JP, Crandall PH. Temporal lobe volumetric cell densities in temporal lobe epilepsy. Epilepsia 1984a; 25: 729-40.
4. Babb TL, Lieb JP, Brown WJ, Pretorius J, Crandall PH. Distribution of pyramidal cell density and hyperexcitability in the epileptic human hippocampal formation. Epilepsia 1984b; 25: 721-8.
5. Bernard-Helary K, Lapouble E, Ardourel M, Hevor T, Cloix JF. Correlation between brain glycogen and convulsive state in mice submitted to methionine sulfoximine. Life Sci 2000; 67: 1773-81.
6. Bertram EH, Williamson JM, Cornett JF, Chen ZF. Design and construction of a long-term continuous video-EEG monitoring unit for simultaneous recording of multiple small animals. Brain Res Brain Res Protoc 1997; 1997: 85-97.
7. Binder DK, Steinhauser C. Functional changes in astroglial cells in epilepsy. Glia 2006; 54: 358-68.
8. Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 1984; 81: 1189-92.
9. Cavus I, Kasoff WS, Cassaday MP, Jacob R, Gueorguieva R, Sherwin RS, et al. Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann Neurol 2005; 57: 226-35.
10. Clifford DB, Zorumski CF, Olney JW. Ketamine and MK-801 prevent degeneration of thalamic neurons induced by focal cortical seizures. Exp Neurol 1989; 105: 272-9.
11. de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, et al. A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 2003; 44: 677-87.
12. de Lanerolle NC, Lee TS. New facets of the neuropathology and molecular profile of human temporal lobe epilepsy. Epilepsy Behav 2005; 7: 190-203.
13. Du F, Whetsell WO Jr, Abou-Khalil B, Blumenkopf B, Lothman EW, Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res 1993; 16: 223-33.
14. During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993; 341: 1607-10.
15. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjornsen LP, Spencer DD, et al. Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci USA 2005; 102: 1193-8.
16. Eid T, Thomas MJ, Spencer DD, Runden-Pran E, Lai JC, Malthankar GV, et al. Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 2004; 363: 28-37.
17. Folbergrova J, Passonneau JV, Lowry OH, Schulz DW. Glycogen, ammonia and related metabolities in the brain during seizures evoked by methionine sulphoximine. J Neurochem 1969; 16: 191-203.
18. Gallyas F, Wolff JR, Bottcher H, Zaborsky L. A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol 1980; 55: 299-306.
19. Gloor P. Mesial temporal sclerosis: historical background and an overview from a modern perspective. In: Luders H, editor. Epilepsy surgery. New York: Raven Press; 1991. p. 6889-703.
20. Gloor P. The role of the amygdala in temporal lobe epilepsy. In: Aggleton JP, editor. The amygdala. Neurobiological aspects of emotion, memory, and mental dysfunction. New York: Wiley-Liss; 1992. p. 505-38.
21. Kim JH, Guimaraes PO, Shen M-Y, Masukawa LM, Spencer DD. Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Acta Neuropathol 1990; 80: 41-5.
22. Laake JH, Slyngstad TA, Haug FM, Ottersen OP. Glutamine from glial cells is essential for the maintenance of the nerve terminal pool of glutamate: immunogold evidence from hippocampal slice cultures. J Neurochem 1995; 65: 871-81.
23. Liang SL, Carlson GC, Coulter DA. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci 2006; 26: 8537-48.
24. Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS. Generation and phenotype of a transgenic knockout mouse lacking the mercurial-insensitive water channel aquaporin-4. J Clin Invest 1997; 100: 957-62.
25. Margerison JH, Corsellis JAN. Epilepsy and the temporal lobes. Brain 1966; 89: 499-530.
26. Mathern GW, Babb TL, Armstrong DL. Hippocampal sclerosis. In: Engel J, Pedley TA, editors. Epilepsy: a comprehensive textbook. Philadelphia: Lippincott-Raven; 1997. p. 133-55.
27. McNamara JO. Cellular and molecular basis of epilepsy. J Neurosci 1994; 14: 3413-25.
28. Meldrum BS. Cell damage in epilepsy and the role of calcium in cytotoxicity. Adv Neurol 1986; 44: 849-55.
29. Olney JW. Neurotoxicity of excitatory amino acids. In: McGeer EG, Olney JW, McGeer PL, editors. Kainic acid as a tool in neurobiology. New York: Raven Press; 1978. p. 37-70.
30. Olney JW, Collins RC, Sloviter RS. Excitotoxic mechanims of epileptic brain damage. In: Delgado-Escueta AV, Ward AA Jr, Woodbury DM, Porter RJ, editors. Advances in neurology. New York: Raven Press; 1986. p. 857-77.
31. Olney JW, Sharpe LG, Feigin RD. Glutamate-induced brain damage in infant primates. J Neuropathol Exp Neurol 1972; 31: 464-88.
32. Otis TS, Jahr CE. Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 1998; 18: 7099-110.
33. Patel MN. Oxidative stress, mitochondrial dysfunction, and epilepsy. Free Radic Res 2002; 36: 1139-46.
34. Petito CK, Feldmann E, Pulsinelli WA, Plum F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology 1987; 37: 1281-6.
35. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 1982; 11: 491-8.
36. Racine RJ, Burnham WM, Gartner JG, Levitan D. Rates of motor seizure development in rats subjected to electrical brain stimulation: strain and inter-stimulation interval effects. Electroencephalogr Clin Neurophysiol 1973; 35: 553-6.
37. Ronzio RA, Meister A. Phosphorylation of methionine sulfoximine by glutamine synthetase. Proc Natl Acad Sci USA 1968; 59: 164-70.
38. Shapiro BM, Stadtman ER. The regulation of glutamine synthesis in microorganisms. Annu Rev Microbiol 1970; 24: 501-24.
39. Shaw CA, Bains JS. Synergistic versus antagonistic actions of glutamate and glutathione: the role of excitotoxicity and oxidative stress in neuronal disease. Cell Mol Biol (Noisy-le-grand) 2002; 48: 127-36.
40. Sommer W. Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch Psychiatr Nervenkr 1880; 10: 631-75.
41. Stanimirovic DB, Ball R, Small DL, Muruganandam A. Developmental regulation of glutamate transporters and glutamine synthetase activity in astrocyte cultures differentiated in vitro. Int J Dev Neurosci 1999; 17: 173-84.
42. Subbalakshmi GY, Murthy CR. Effects of methionine sulfoximine on cerebral ATPase. Biochem Pharmacol 1981; 30: 2127-30.
43. Szegedy L. Enzyme histochemical studies in the rat hippocampus, cerebellar cortex and brainstem motor nuclei during methionine sulphoximine convulsions. Cell Mol Biol 1978; 23: 43-53.
44. Turski L, Niemann W, Stephens DN. Differential effects of antiepileptic drugs and beta-carbolines on seizures induced by excitatory amino acids. Neuroscience 1990; 39: 799-807.
45. Wang Y, Zaveri HP, Ghosh A, Beckstrom H, De Lanerolle NC, Eid T. Inhibition of hippocampal glutamine synthetase causes spontaneously recurrent seizures in rats. Epilepsia 2006; 47: 328-329.