Neuronal and glial metabolite content of the epileptogenic human hippocampus

Annals of Neurology

Volumn 52, Issue 5, 2002, Pages 635-642

  Petroff, Ognen A C ^a   Errante, Laura D ^a   Rothman, Douglas L ^b   Kim, Jung H ^a   Spencer, Dennis D ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ASPARTIC ACID; GLUTAMIC ACID; GLUTAMINE; N ACETYLASPARTIC ACID;

ADOLESCENT; ADULT; ARTICLE; BRAIN ATROPHY; BRAIN METABOLISM; CELL LOSS; CELL METABOLISM; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; EPILEPTOGENESIS; GLIA CELL; GLIOSIS; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; LOBECTOMY; MALE; METABOLITE; NERVE CELL; PELIZAEUS MERZBACHER DISEASE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STATISTICAL SIGNIFICANCE; TEMPORAL LOBE EPILEPSY;

ADULT; AMINO ACIDS; ASPARTIC ACID; EPILEPSY, TEMPORAL LOBE; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLUTAMINE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROGLIA; NEURONS;

EID: 0036828818     PISSN: 03645134     EISSN: None     Source Type: Journal    
DOI: 10.1002/ana.10360     Document Type: Article

References (73)

1. Jackson G, Van Paesschen W. Hippocampal sclerosis in the MR era. Epilepsia 2002;43(suppl 1):4-10.
2. Dalby NO, Mody I. The process of epileptogenesis: A pathophysiological approach. Curr Opin Neurol 2001;14:187-192.
3. Cascino GD. Advances in neuroimaging: Surgical localization. Epilepsia 2001;42:3-12.
4. Mathern GW, Babb TL, Armstrong DL. Hippocampal sclerosis. In: Engel J, Pedley TA, eds. Epilepsy a Comprehensive Textbook. Philadelphia: Lippincott-Raven, 1997:133-156.
5. Kim JH, Guimaraes PO, Shen MY, et al. Hippocampal neuronal density in temporal lobe epilepsy with and without gliomas. Acta Neuropathol 1990;80:41-45.
6. Luby M, Spencer DD, Kim JH, et al. Hippocampal MRI volumetrics and temporal lobe substrates in medial temporal lobe epilepsy. Magn Reson Imaging 1995;13:1065-1071.
7. Duncan JS. Imaging and epilepsy. Brain 1997;120:339-377.
8. Bronen RA, Knowlton R, Garwood M, et al. High-resolution imaging in epilepsy. Epilepsia 2002;43(suppl 1):11-18.
9. Kuzniecky R, Palmer C, Hugg J, et al. Magnetic resonance spectroscopic imaging in temporal lobe epilepsy: Neuronal dysfunction or cell loss? Arch Neurol 2001;58:2048-2053.
10. Diehl B, Najm I, Mohamed A, et al. Fluid-attenuated inversion recovery: Correlations of hippocampal cell densities with signal abnormalities. Neurology 2001;57:1029-1032.
11. Van Paesschen W, Revesz T, Duncan JS, et al. Quantitative neuropathology and quantitative magnetic resonance imaging of the hippocampus in temporal lobe epilepsy. Ann Neurol 1997;42:756-766.
12. Henry TR. PET: cerebral blood flow and glucose metabolism-presurgical localization. Adv Neutol 2000;83:105-120.
13. Spanaki MV, Kopylev L, DeCarli C, et al. Postoperative changes in cerebral metabolism in temporal lobe epilepsy. Arch Neurol 2000;57:1447-1452.
14. Theodore WH, Gaillard WD, De Carli C, et al. Hippocampal volume and glucose metabolism in temporal lobe epileptic foci. Epilepsia 2001;42:130-132.
15. Foldvary N, Lee N, Hanson MW, et al. Correlation of hippocampal neuronal density and FDG-PET in mesial temporal lobe epilepsy. Epilepsia 1999;40:26-29.
16. Lamusuo S, Jutila L, Ylinen A, et al. [18F]FDG-PET reveals temporal hypometabolism in patients with temporal lobe epilepsy even when quantitative MRI and histopathological analysis show only mild hippocampal damage. Arch Neurol 2001;58:933-939.
17. Brines ML, Tabuceau H, Sundaresan S, et al. Regional distributions of hippocampal Na+,K(+)-ATPase, cytochrome oxidase, and total protein in temporal lobe epilepsy. Epilepsia 1995;36:371-383.
18. Hugg JW, Laxer KD, Matson GB, et al. Neuron loss localizes human temporal lobe epilepsy by in vivo proton magnetic resonance spectroscopic imaging. Ann Neurol 1993;34:788-794.
19. Gadian DG, Connelly A, Duncan JS, et al. 1H magnetic resonance spectroscopy in the investigation of intractable epilepsy. Acta Neurol Scand 1994;152(suppl):116-121.
20. Cendes F, Caramanos Z, Andermann F, et al. Proton magnetic resonance spectroscopic imaging and magnetic resonance imaging volumetry in the lateralization of temporal lobe epilepsy: A series of 100 patients. Ann Neurol 1997;42:737-746.
21. Cendes F, Knowlton RC, Novotny EJ, et al. Magnetic resonance spectroscopy in epilepsy: Clinical issues. Epilepsia 2002;43(suppl 1):32-39.
22. Lu D, Margouleff C, Rubib E, et al. Temporal lobe epilepsy: Correlation of proton magnetic resonance spectroscopy and 18F-fluorodeoxyglucose positron emission tomography. Magn Reson Med 1997:37:18-23.
23. Hugg JW, Kuzniecky RI, Gilliam FG, et al. Normalization of contralateral metabolic function following temporal lobectomy demonstrated by 1H magnetic resonance spectroscopic imaging. Ann Neurol 1996;40:236-239.
24. Cendes F, Andermann F, Dubeau F, et al. Normalization of neuronal metabolic dysfunction after surgery for temporal lobe epilepsy. Evidence from proton spectroscopic imaging. Neurology 1997;49:1525-1533.
25. Connelly A, Van Paesschen W, Porter DA, et al. Proton magnetic resonance spectroscopy in MRI-negative temporal lobe epilepsy. Neurology 1998;51:61-66.
26. Woermann FG, McLean MA, Bartlett PA, et al. Short echo time single-voxel H-1 magnetic resonance spectroscopy in magnetic resonance imaging negative temporal lobe epilepsy: Different biochemical profile compared with hippocampal sclerosis. Ann Neurol 1999;45:369-376.
27. Savic I, Thomas AM, Ke Y, et al. In vivo measurements of glutamine plus glutamate (Glx) and N-aceryl aspartate (NAA) levels in human partial epilepsy. Acta Neurol Scand 2000;102:179-187.
28. Mueller SG, Weber OM, Duc CO, et al. Effects of vigabatrin on brain GABA plus/CR signals in patients with epilepsy monitored by H-1-NMR-spectroscopy: Responder characteristics. Epilepsia 2001;42:29-40.
29. Duc CO, Trabesinger AH, Weber OM, et al. Quantitative 1H MRS in the evaluation of mesial temporal lobe epilepsy in vivo. Magn Reson Imaging 1998;16:969-979.
30. Petroff OAC, Errante LD, Kim JH, et al. Glutamine synthesis and glutamate-glutamine cycling are low in patients with hippocampal sclerosis. Epilepsia 2000;41(suppl 7):160.
31. Petroff OAC, Spencer D, Alger JR, Prichard JW. High-field proton magnetic resonance spectroscopy of human cerebrum obtained during surgery for epilepsy. Neurology 1989;39:1197-1202.
32. Petroff OAC, Pleban LA, Spencer DD. Symbiosis between in vivo and in vitro NMR spectroscopy: The creatine, N-acetyl aspartate, glutamate, and GABA content of epileptic human brain. Magn Reson Imaging 1995;13:1197-1211.
33. Spencer SS, Kim J, deLanerolle N, Spencer DD. Differential neuronal and glial relations with parameters of ictal discharge in mesial temporal lobe epilepsy. Epilepsia 1999;40:708-712.
34. Altman DG. Practical Statistics for Medical Research. London: Chapman & Hall, 1991.
35. Tsai G, Coyle JT. N-acetyl aspartate in neuropsychiatric disorders. Prog Neurobiol 1995;46:531-540.
36. Bates TE, Strangward M, Keelan J, et al. Inhibition of N-acetyl aspartate production: Implications for 1H MRS studies in vivo. Neuroreport 1996;7:1397-1422.
37. Clark JB, N-acetyl aspartate: A marker for neuronal loss or mitochondrial dysfunction. Dev Neurosci 1998;20:271-276.
38. Baslow MH. Functions of N-acetyl-L-aspartate and N-acetyl-Laspartylglutamate in the vertebrate brain: Role in glial cell-specific signaling. J Neurochem 2000;75:453-459.
39. Peeling J, Sutherland G. 1H magnetic resonance spectroscopy of extracts of human epileptic neocortex and hippocampus. Neurology 1993;43:589-594.
40. Choi CG, Frahm J. Localized proton MRS of the human hippocampus: Metabolite concentrations and relaxation times. Magn Reson Med 1999;41:204-207.
41. McLean MA, Woermann FG, Simister RJ, et al. In vivo short echo time 1H-magnetic resonance spectroscopic imaging (MRSI) of the temporal lobes. Neuroimage 2001;14:501-509.
42. Jaarsma D, Veenma-van der Duin L, Korf J. N-acetyl aspartate and N-acetylasparrylglutamate levels in Alzheimer's disease post-mortem brain tissue. J Neurol Sci 1994;127:230-233.
43. Tsai G, Passani LA, Slusher BS, et al. Abnormal excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiat 1995;52:829-836.
44. Mohanakrishnan P, Fowler AH, Vonsattel JP, et al. Regional metabolic alterations in Alzheimer's disease: An in vitro 1H NMR study of the hippocampus and cerebellum. J Gerontol 1997;52:B111-B117.
45. Petroff OAC, Ogino T, Alger JR. High-resolution proton magnetic resonance spectroscopy of rabbit brain: Regional metabolites levels and post-mortem changes. J Neurochem 1988;51:163-171.
46. Perry TL, Hansen S, Gandham SS. Postmortem changes of amino compounds in human and rat brain. J Neurochem 1981;36:406-412.
47. Tarbit I, Perry EK, Perry RH, et al. Hippocampal free amino acids in Alzheimer's disease. J Neurochem 1980;35:1246-1249.
48. Ellison DW, Beal MF, Mazurek MF, et al. A postmortem study of amino acid neurotransmitters in Alzheimer's disease. Ann Neurol 1986;20:616-621.
49. Sasaki H, Muramoto O, Arai H, et al. Regional distribution of amino acid transmitters in postmortem brains of presenile and senile dementia of Alzheimer type. Ann Neurol 1986;20:263-269.
50. Behar KL, den Hollander JA, Stromski ME, et al. High-resolution 1H IH nuclear magnetic resonance study of cerebral hypoxia in vivo. Proc Nad Acad Sci USA 1983;80:4945-4948.
51. Kerr SE, Ghantus M. The carbohydrate metabolism of brain. III. On the origin of lactic acid. J Biol Chem 1937;117:217-225.
52. Lowry OH, Berger SJ, Chi M M-Y, et al. Diversity of metabolic patterns in human brain tumors. I. High energy phosphate compounds and basic composition. J Neurochem 1977;29:959-977.
53. Sherwin AL. Neuroactive amino acids in focally epileptic human brain: A review. Neurochem Res 1999;124:1387-1395.
54. Petroff OAC, Pan JW, Rothman DL. Magnetic resonance spectroscopic studies of neurotransmitters and energy metabolism in epilepsy. Epilepsia 2002;43(suppl 1):40-50.
55. During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 1993;341:1607-1613.
56. Wilson CL, Maidment NT, Shomer MH, et al. Comparison of seizure related amino acid release in human epileptic hippocampus versus a chronic, kainate rat model of hippocampal epilepsy. Epilepsy Res 1996;26:245-254.
57. Shen J, Petersen KF, Behar KL, et al. Determination of the rate of the glutamate-glutamine cycle in human brain by in vivo 13C NMR. Proc Soc Nad Acad Sci USA 1999;96:8235-8240.
58. Sibson NR, Mason GF, Shen J, et al. In vivo (13)C NMR measurement of neurotransmitter glutamate cycling, anaplerosis and TCA cycle flux in rat brain during [2-13C]glucose infusion. J Neurochem 2001;76:975-989.
59. Moreno A, Ross BD, Bluml S. Direct determination of the N-acetyl-L-aspartate synthesis rate in the human brain by (13)C MRS and [1-(13)C]glucose infusion. J Neurochem 2001;77: 347-350.
60. Petroff OAC, Pan JW, Rothman DL. Magnetic resonance spectroscopic studies of neurotransmitters and energy metabolism in epilepsy. Epilepsia 2002;43(suppl 1):40-50.
61. Lebon V, Petersen KF, Cline GW, et al. Astroglial contribution to brain energy metabolism in humans revealed by 13C nuclear magnetic resonance spectroscopy: Elucidation of the dominant pathway for neurotransmitter glutamate repletion and measurement of astrocytic oxidative metabolism. J Neurosci 2002;22: 1523-1531.
62. Maragakis NJ, Rothstein JD. Glutamate transporters in neurologic disease. Arch Neurol 2001;58:365-370.
63. Danbolt NC. Glutamate uptake. Prog Neurobiol 2001;65:1-105.
64. Hanu R, McKenna M, O'Neill A, et al. Monocarboxylic acid transporters, MCT1 and MCT2, in cortical astrocytes in vitro and in vivo. Am J Physiol Cell Physiol 2000;278:C921-C930.
65. Bluml S, Moreno-Torres A, Shic F, et al. Tricarboxylic acid cycle of glia in the in vivo human brain. NMR Biomed 2002;15:1-5.
66. Sager TN, Thomsen C, Valsborg JS, et al. Astroglia contain a specific transport mechanism for N-acetyl-L-aspartate. J Neurochem 1999;73:807-811.
67. Huang W, Wang H, Kekuda R, et al. Transport of N-acetyl aspartate by the Na(+)-dependent high-affinity dicarboxylate transporter NaDC3 and its relevance to the expression of the transporter in the brain. J Pharmacol Exp Ther 2000;295:392-403.
68. Chakraborty G, Mekala P, Yahya D, et al. Intraneuronal N-acetyl aspartate supplies acetyl groups for myelin lipid synthesis: Evidence for myelin-associated aspartoacylase. J Neurochem 2001;78:736-745.
69. Baslow MH, Suckow RF, Sapirstein V, Hungund BL. Expression of aspartoacylase activity in cultured rat macroglial cells is limited to oligodendrocytes. J Mol Neurosci 1999;13: 47-53.
70. Urenjak J, Williams SR, Gadian DG, Noble M. Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci 1993;13:981-989.
71. Bhakoo KK, Pearce D. In vitro expression of N-acetyl aspartate by oligodendrocytes: Implications for proton magnetic resonance spectroscopy signal in vivo. J Neurochem 2000;74:254-262.
72. Hyder F, Kida I, Behar KL, et al. Quantitative functional imaging of the brain: Towards mapping neuronal activity by BOLD fMRI. NMR Biomed 2001;14:413-431.
73. Lieth E, LaNoue KF, Berkich DA, et al. Nitrogen shuttling between neurons and glial cells during glutamate synthesis. J Neurochem 2001;76:1712-1723.