Gene expression of glutamate metabolizing enzymes in the hippocampal formation in human temporal lobe epilepsy

Epilepsia

Volumn 54, Issue 2, 2013, Pages 228-238

  Eid, Tore ^a   Lee, Tih Shih W ^a   Wang, Yue ^a   Peréz, Edgar ^a   Drummond, Jana ^b   Lauritzen, Fredrik ^a,c   Bergersen, Linda H ^c   Meador Woodruff, James H ^b   Spencer, Dennis D ^a   De Lanerolle, Nihal C ^a   McCullumsmith, Robert E ^b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Astrocytes; Brain; Glutamate glutamine cycle; Glutamine synthetase; Phosphate activated glutaminase

Indexed keywords

CARBAMAZEPINE; CLONAZEPAM; CLORAZEPATE; GLUTAMATE AMMONIA LIGASE; GLUTAMINASE; LAMOTRIGINE; MESSENGER RNA; PHENOBARBITAL; PHENYLEPHRINE; PHENYTOIN; PHOSPHATE ACTIVATED GLUTAMINASE; PRIMIDONE; TOPIRAMATE; UNCLASSIFIED DRUG; VALPROIC ACID;

ADULT; ARTICLE; ASTROCYTOMA; AUTOPSY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DENTATE HILUS; ENZYME MECHANISM; FEMALE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLIOBLASTOMA; GLIOMA; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL SCLEROSIS; HUMAN; HUMAN TISSUE; IN SITU HYBRIDIZATION; MALE; MOLECULAR MECHANICS; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE IMAGING; PELIZAEUS MERZBACHER DISEASE; PRIORITY JOURNAL; REGULATORY MECHANISM; SCHOOL CHILD; SUBICULUM; TEMPORAL LOBE EPILEPSY;

ADOLESCENT; ADULT; AUTOPSY; CHILD; ELECTROENCEPHALOGRAPHY; EPILEPSY, TEMPORAL LOBE; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUTAMATE-AMMONIA LIGASE; GLUTAMIC ACID; GLUTAMINASE; HIPPOCAMPUS; HUMANS; IN SITU HYBRIDIZATION; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; RNA, MESSENGER; YOUNG ADULT;

EID: 84873407989     PISSN: 00139580     EISSN: 15281167     Source Type: Journal    
DOI: 10.1111/epi.12008     Document Type: Article

References (62)

1. Albrecht P, Lewerenz J, Dittmer S, Noack R, Maher P, Methner A,. (2010) Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system xc- as a neuroprotective drug target. CNS Neurol Disord Drug Targets 9: 373-382.
2. Amaral DG, Insausti R,. (1990) Hippocampal formation. In, Paxinos G, (Ed.) The human nervous system. Academic Press, San Diego, CA, pp. 711-756.
3. Ben-Ari Y,. (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14: 375-403.
4. Berg M, Bruhn T, Johansen FF, Diemer NH,. (1993) Kainic acid-induced seizures and brain damage in the rat: different effects of NMDA- and AMPA receptor antagonists. Pharmacol Toxicol 73: 262-268.
5. Bidmon HJ, Gorg B, Palomero-Gallagher N, Schleicher A, Haussinger D, Speckmann EJ, Zilles K,. (2008) Glutamine synthetase becomes nitrated and its activity is reduced during repetitive seizure activity in the pentylentetrazole model of epilepsy. Epilepsia 49: 1733-1748.
6. Binder DK, Oshio K, Ma T, Verkman AS, Manley GT,. (2004) Increased seizure threshold in mice lacking aquaporin-4 water channels. NeuroReport 15: 259-262.
7. Binder DK, Nagelhus EA, Ottersen OP,. (2012) Aquaporin-4 and epilepsy. Glia 60: 1203-1214.
8. Bordey A, Sontheimer H,. (1998) Properties of human glial cells associated with epileptic seizure foci. Epilepsy Res 32: 286-303.
9. Boyd-Kimball D, Sultana R, Poon HF, Lynn BC, Casamenti F, Pepeu G, Klein JB, Butterfield DA,. (2005) Proteomic identification of proteins specifically oxidized by intracerebral injection of amyloid beta-peptide (1-42) into rat brain: implications for Alzheimer's disease. Neuroscience 132: 313-324.
10. Bruneau EG, McCullumsmith RE, Haroutunian V, Davis KL, Meador-Woodruff JH,. (2005) Increased expression of glutaminase and glutamine synthetase mRNA in the thalamus in schizophrenia. Schizophr Res 75: 27-34.
11. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, Butterfield DA,. (2002) Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 33: 562-571.
12. Cavus I, Kasoff WS, Cassaday MP, Jacob R, Gueorguieva R, Sherwin RS, Krystal JH, Spencer DD, Abi-Saab WM,. (2005) Extracellular metabolites in the cortex and hippocampus of epileptic patients. Ann Neurol 57: 226-235.
13. Cavus I, Pan JW, Hetherington HP, Abi-Saab W, Zaveri HP, Vives KP, Krystal JH, Spencer SS, Spencer DD,. (2008) Decreased hippocampal volume on MRI is associated with increased extracellular glutamate in epilepsy patients. Epilepsia 49: 1358-1366.
14. Clinton SM, Haroutunian V, Davis KL, Meador-Woodruff JH,. (2003) Altered transcript expression of NMDA receptor-associated postsynaptic proteins in the thalamus of subjects with schizophrenia. Am J Psychiatry 160: 1100-1109.
15. de Lanerolle NC, Kim JH, Robbins RJ, Spencer DD,. (1989) Hippocampal interneuron loss and plasticity in human temporal lobe epilepsy. Brain Res 495: 387-395.
16. de Lanerolle NC, Brines ML, Kim JH, Williamson A, Philips MF, Spencer DD,. (1992) Neurochemical remodelling of the hippocampus in human temporal lobe epilepsy. In, Engel J Jr, Wasterlain C, Cavalheiro EA, Heinemann U, Avanzini G, (Eds) Molecular neurobiology of epilepsy. Elsevier Science Publishers, B.V., Amsterdam, pp. 205-220.
17. de Lanerolle NC, Kim JH, Williamson A, Spencer SS, Zaveri HP, Eid T, Spencer DD,. (2003) A retrospective analysis of hippocampal pathology in human temporal lobe epilepsy: evidence for distinctive patient subcategories. Epilepsia 44: 677-687.
18. Downs AM, Williams MA,. (1984) An improved approach to the analysis of autoradiographs containing isolated sources of simple shape: method, theoretical basis and reference data. J Microsc 136: 1-22.
19. During MJ, Spencer DD,. (1993) Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 341: 1607-1610.
20. Eid T, Coulter DA,. (2012) Astrocytic regulation of glutamate homeostasis in epilepsy. Glia 60: 1215-1226.
21. Eid T, Du F, Schwarcz R,. (1995) Differential neuronal vulnerability to amino-oxyacetate and quinolinate in the rat parahippocampal region. Neuroscience 68: 645-656.
22. Eid T, Thomas MJ, Spencer DD, Runden-Pran E, Lai JC, Malthankar GV, Kim JH, Danbolt NC, Ottersen OP, de Lanerolle NC,. (2004) Loss of glutamine synthetase in the human epileptogenic hippocampus: possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363: 28-37.
23. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjornsen LP, Spencer DD, Agre P, Ottersen OP, de Lanerolle NC,. (2005) Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci USA 102: 1193-1198.
24. Eid T, Hammer J, Runden-Pran E, Roberg B, Thomas MJ, Osen K, Davanger S, Laake P, Torgner IA, Lee TS, Kim JH, Spencer DD, Ottersen OP, de Lanerolle NC,. (2007) Increased expression of phosphate-activated glutaminase in hippocampal neurons in human mesial temporal lobe epilepsy. Acta Neuropathol 113: 137-152.
25. Eid T, Ghosh A, Wang Y, Beckstrom H, Zaveri HP, Lee TS, Lai JC, Malthankar-Phatak GH, de Lanerolle NC,. (2008a) Recurrent seizures and brain pathology after inhibition of glutamine synthetase in the hippocampus in rats. Brain 131: 2061-2070.
26. Eid T, Williamson A, Lee TS, Petroff OA, de Lanerolle NC,. (2008b) Glutamate and astrocytes-key players in human mesial temporal lobe epilepsy? Epilepsia 49 (Suppl. 2): 42-52.
27. Eid T, Behar K, Dhaher R, Bumanglag AV, Lee TS,. (2012) Roles of glutamine synthetase inhibition in epilepsy. Neurochem Res Apr 10 [Epub ahead of print].
28. Engel J, Williamson PD, Wieser HG,. (2008) Mesial temporal lobe epilepsy with hippocampal sclerosis. In, Engel J, Pedley TA, (Eds) Epilepsy: a comprehensive textbook. Wolters Kluver, Lippincott Williams & Wilkins, Philadelphia, PA, pp. 2479-2486.
29. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO,. (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11: 4241-4257.
30. Gloor P,. (1991) Mesial temporal sclerosis: historical background and an overview from a modern perspective. In, Luders H, (Ed.) Epilepsy surgery. Raven Press, New York, pp. 689-703.
31. Hayashi T,. (1954) Effects of sodium glutamate on the nervous system. Keiko J Med 3: 183-192.
32. Hinterkeuser S, Schroder W, Hager G, Seifert G, Blumcke I, Elger CE, Schramm J, Steinhauser C,. (2000) Astrocytes in the hippocampus of patients with temporal lobe epilepsy display changes in potassium conductances. Eur J Neurosci 12: 2087-2096.
33. Houser CR, Miyashiro JE, Swartz BE, Walsh GO, Rich JR, Delgado-Escueta AV,. (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganization in human hippocampal epilepsy. J Neurosci 10: 267-282.
34. Ibrahim HM, Hogg AJ Jr, Healy DJ, Haroutunian V, Davis KL, Meador-Woodruff JH,. (2000) Ionotropic glutamate receptor binding and subunit mRNA expression in thalamic nuclei in schizophrenia. Am J Psychiatry 157: 1811-1823.
35. Ikeda E, Achen MG, Breier G, Risau W,. (1995) Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem 270: 19761-19766.
36. Iserhot C, Gebhardt C, Schmitz D, Heinemann U,. (2004) Glutamate transporters and metabotropic receptors regulate excitatory neurotransmission in the medial entorhinal cortex of the rat. Brain Res 1027: 151-160.
37. Laake JH, Takumi Y, Eidet J, Torgner IA, Roberg B, Kvamme E, Ottersen OP,. (1999) Postembedding immunogold labelling reveals subcellular localization and pathway-specific enrichment of phosphate activated glutaminase in rat cerebellum. Neuroscience 88: 1137-1151.
38. Lee TS, Eid T, Mane S, Kim JH, Spencer DD, Ottersen OP, de Lanerolle NC,. (2004) Aquaporin-4 is increased in the sclerotic hippocampus in human temporal lobe epilepsy. Acta Neuropathol 108: 493-502.
39. Lorente de Nõ R,. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46: 113-177.
40. Lucas DR, Newhouse JP,. (1957) The toxic effect of sodium L-glutamate on the inner layers of the retina. AMA Arch Ophthalmol 58: 193-201.
41. Martinez-Hernandez A, Bell KP, Norenberg MD,. (1977) Glutamine synthetase: glial localization in brain. Science 195: 1356-1358.
42. Mathern GW, Babb TL, Armstrong DL,. (1997) Hippocampal sclerosis. In, Engel J, Pedley TA, (Eds) Epilepsy: a comprehensive textbook. Lippincott-Raven, Philadelphia, PA, pp. 133-155.
43. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Dehnes Y, Danbolt NC, Nelson N, Leite JP, Chimelli L, Born DE, Sakamoto AC, Assirati JA, Fried I, Peacock WJ, Ojemann GA, Adelson PD,. (1999) Hippocampal GABA and glutamate transporter immunoreactivity in patients with temporal lobe epilepsy. Neurology 52: 453-472.
44. McCullumsmith RE, Meador-Woodruff JH,. (2011) Novel approaches to the study of postmortem brain in psychiatric illness: old limitations and new challenges. Biol Psychiatry 69: 127-133.
45. McNamara RK, Routtenberg A,. (1995) NMDA receptor blockade prevents kainate induction of protein F1/GAP-43 mRNA in hippocampal granule cells and subsequent mossy fiber sprouting in the rat. Brain Res Mol Brain Res 33: 22-28.
46. Mochizuki H, Murphy CJ, Brandt JD, Kiuchi Y, Russell P,. (2012) Altered stability of mRNAs associated with glaucoma progression in human trabecular meshwork cells following oxidative stress. Invest Ophthalmol Vis Sci 53: 1734-1741.
47. Molinari F, Cattani AA, Mdzomba JB, Aniksztejn L,. (2012) Glutamate transporters control metabotropic glutamate receptors activation to prevent the genesis of paroxysmal burst in the developing hippocampus. Neuroscience 207: 25-36.
48. Olney JW, Sharpe LG, Feigin RD,. (1972) Glutamate-induced brain damage in infant primates. J Neuropathol Exp Neurol 31: 464-488.
49. Olney JW, Collins RC, Sloviter RS,. (1986) Excitotoxic mechanims of epileptic brain damage. In, Delgado-Escueta AV, Ward AA Jr, Woodbury DM, Porter RJ, (Eds) Advances in neurology. Raven Press, New York, pp. 857-877.
50. Otis TS, Jahr CE,. (1998) Anion currents and predicted glutamate flux through a neuronal glutamate transporter. J Neurosci 18: 7099-7110.
51. Petroff OA, Cavus I, Kim JH, Spencer DD,. (2004) Interictal extracellular glutamate concentrations are increased in hippocampal sclerosis. Ann Neurol 56: S43.
52. Proper EA, Hoogland G, Kappen SM, Jansen GH, Rensen MG, Schrama LH, van Veelen CW, van Rijen PC, van Nieuwenhuizen O, Gispen WH, de Graan PN,. (2002) Distribution of glutamate transporters in the hippocampus of patients with pharmaco-resistant temporal lobe epilepsy. Brain 125: 32-43.
53. Sheng JG, Boop FA, Mrak RE, Griffin WS,. (1994) Increased neuronal beta-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1 alpha immunoreactivity. J Neurochem 63: 1872-1879.
54. Sommer W,. (1880) Erkrankung des Ammonshorns als aetiologisches Moment der Epilepsie. Arch Psychiatr Nervenkr 10: 631-675.
55. Spencer DD, Spencer SS,. (1991) Surgery for epilepsy. Blackwell Scientific Publishers, Boston, MA.
56. Spencer DD, Spencer SS, Mattson RH, Williamson PD, Novelly R,. (1984) Access to posterior medial temporal lobe structures in the surgical treatment of temporal lobe epilepsy. Neurosurgery 15: 667-671.
57. Svenneby G,. (1970) Pig brain glutaminase: purification and identification of different enzyme forms. J Neurochem 17: 1591-1599.
58. 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.
59. van der Hel WS, Notenboom RG, Bos IW, van Rijen PC, van Veelen CW, de Graan PN,. (2005) Reduced glutamine synthetase in hippocampal areas with neuron loss in temporal lobe epilepsy. Neurology 64: 326-333.
60. Wang Y, Zaveri HP, Lee TS, Eid T,. (2009) The development of recurrent seizures after continuous intrahippocampal infusion of methionine sulfoximine in rats: a video-intracranial electroencephalographic study. Exp Neurol 220: 293-302.
61. Watanabe T, Morimoto K, Hirao T, Suwaki H, Watase K, Tanaka K,. (1999) Amygdala-kindled and pentylenetetrazole-induced seizures in glutamate transporter GLAST-deficient mice. Brain Res 845: 92-96.
62. Williams MA,. (1982) Autoradiography: its methodology at the present time. J Microsc 128: 79-94.