Inhibitory networks in epilepsy-associated gangliogliomas and in the perilesional epileptic cortex

Epilepsy Research

Volumn 74, Issue 1, 2007, Pages 33-44

  Aronica, E ^a   Redeker, S ^a   Boer, K ^a   Spliet, W G M ^b   van Rijen, P C ^c   Gorter, J A ^d,e   Troost, D ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

^e STICHTING EPILEPSIE INSTELLINGEN NEDERLAND SEIN   (Netherlands)

Author keywords

GABA; Glioneuronal tumors; Immunocytochemistry; Interneurons; Malformations of cortical development; Receptors

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID TRANSPORTER 1; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; PARVALBUMIN; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ARTICLE; BRAIN CORTEX; CELL DENSITY; CONTROLLED STUDY; EPILEPSY; FEMALE; GLIA CELL; GLIOMA; HUMAN; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; PERILESIONAL CORTEX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

ADOLESCENT; ADULT; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBRAL CORTEX; EPILEPSY, TEMPORAL LOBE; FEMALE; GABA PLASMA MEMBRANE TRANSPORT PROTEINS; GANGLIOGLIOMA; HUMANS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MIDDLE AGED; PARVALBUMINS; PROTEINS; RECEPTORS, GABA-A; RECEPTORS, GABA-B;

EID: 33947143011     PISSN: 09201211     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.eplepsyres.2006.12.002     Document Type: Article

References (62)

1. Alonso-Nanclares L., and De Felipe J. Vesicular glutamate transporter 1 immunostaining in the normal and epileptic human cerebral cortex. Neuroscience 134 (2005) 59-68
2. Alonso-Nanclares L., Garbelli R., Sola R.G., Pastor J., Tassi L., Spreafico R., and DeFelipe J. Microanatomy of the dysplastic neocortex from epileptic patients. Brain 128 (2005) 158-173
3. Aronica E., Gorter J.A., Jansen G.H., Leenstra S., Yankaya B., and Troost D. Expression of connexin 43 and connexin 32 gap-junction proteins in epilepsy-associated brain tumors and in the perilesional epileptic cortex. Acta Neuropathol. (Berl) 101 (2001) 449-459
4. Aronica E., Gorter J.A., Jansen G.H., van Veelen C.W., van Rijen P.C., Ramkema M., and Troost D. Expression and cell distribution of group I and group II metabotropic glutamate receptor subtypes in taylor-type focal cortical dysplasia. Epilepsia 44 (2003) 785-795
5. Aronica E., Leenstra S., van Veelen C.W., van Rijen P.C., Hulsebos T.J., Tersmette A.C., Yankaya B., and Troost D. Glioneuronal tumors and medically intractable epilepsy: a clinical study with long-term follow-up of seizure outcome after surgery. Epilepsy Res. 43 (2001) 179-191
6. Aronica E., Yankaya B., Jansen G.H., Leenstra S., van Veelen C.W., Gorter J.A., and Troost D. Ionotropic and metabotropic glutamate receptor protein expression in glioneuronal tumors from patients with intractable epilepsy. Neuropathol. Appl. Neurobiol. 27 (2001) 1-16
7. Avoli M., Louvel J., Pumain R., and Kohling R. Cellular and molecular mechanisms of epilepsy in the human brain. Progr. Neurobiol. 77 (2005) 166-200
8. Baimbridge K.G., Celio M.R., and Rogers J.H. Calcium-binding proteins in the nervous system. Trends Neurosci. 15 (1992) 303-308
9. Barkovich A.J., Kuzniecky R.I., Jackson G.D., Guerrini R., and Dobyns W.B. A developmental and genetic classification for malformations of cortical development. Neurology 65 (2005) 1873-1887
10. Bettler B., Kaupmann K., Mosbacher J., and Gassmann M. Molecular structure and physiological functions of GABA(B) receptors. Physiol. Rev. 84 (2004) 835-867
11. Blumcke I., Lobach M., Wolf H.K., and Wiestler O.D. Evidence for developmental precursor lesions in epilepsy-associated glioneuronal tumors. Microsc. Res. Tech. 46 (1999) 53-58
12. Blumcke I., and Wiestler O.D. Gangliogliomas: an intriguing tumor entity associated with focal epilepsies. J. Neuropathol. Exp. Neurol. 61 (2002) 575-584
13. Calcagnotto M.E., Paredes M.F., Tihan T., Barbaro N.M., and Baraban S.C. Dysfunction of synaptic inhibition in epilepsy associated with focal cortical dysplasia. J. Neurosci. 25 (2005) 9649-9657
14. Cepeda C., Andre V.M., Flores-Hernandez J., Nguyen O.K., Wu N., Klapstein G.J., Nguyen S., Koh S., Vinters H.V., Levine M.S., and Mathern G.W. Pediatric cortical dysplasia: correlations between neuroimaging, electrophysiology and location of cytomegalic neurons and balloon cells and glutamate/GABA synaptic circuits. Dev. Neurosci. 27 (2005) 59-76
15. Charles K.J., Deuchars J., Davies C.H., and Pangalos M.N. GABA B receptor subunit expression in glia. Mol. Cell. Neurosci. 24 (2003) 214-223
16. Cobos I., Calcagnotto M.E., Vilaythong A.J., Thwin M.T., Noebels J.L., Baraban S.C., and Rubenstein J.L. Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat. Neurosci. 8 (2005) 1059-1068
17. Conti F., Melone M., De Biasi S., Minelli A., Brecha N.C., and Ducati A. Neuronal and glial localization of GAT-1, a high-affinity gamma-aminobutyric acid plasma membrane transporter, in human cerebral cortex: with a note on its distribution in monkey cortex. J. Compar. Neurol. 396 (1998) 51-63
18. Conti F., Minelli A., and Melone M. GABA transporters in the mammalian cerebral cortex: localization, development and pathological implications. Brain Res. -Brain Res. Rev. 45 (2004) 196-212
19. Crino P.B., Duhaime A.C., Baltuch G., and White R. Differential expression of glutamate and GABA-A receptor subunit mRNA in cortical dysplasia. Neurology 56 (2001) 906-913
20. D'Antuono M., Louvel J., Kohling R., Mattia D., Bernasconi A., Olivier A., Turak B., Devaux A., Pumain R., and Avoli M. GABAA receptor-dependent synchronization leads to ictogenesis in the human dysplastic cortex. Brain 127 (2004) 1626-1640
21. de Jongh A., de Munck J.C., Baayen J.C., Puligheddu M., Jonkman E.J., and Stam C.J. Localization of fast MEG waves in patients with brain tumors and epilepsy. Brain Topogr. 15 (2003) 173-179
22. DeFelipe J., Hendry S.H., and Jones E.G. Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 2093-2097
23. Engel J.J. Outcome with respect to epileptic seizures. In: Engel J.J. (Ed). Surgical Treatment of the Epilepsies (1993), Raven Press, New York 609-621
24. Farrell M.A., and Vinters H.V. General neuropathology of epilepsy. In: Engel J., and Pedley T.A. (Eds). Epilepsy: A Comprehensive Textbook (1997), Lippincott-Raven, Philadelphia 157-174
25. Ferrer I., Oliver B., Russi A., Casas R., and Rivera R. Parvalbumin and calbindin-D28k immunocytochemistry in human neocortical epileptic foci. J. Neurol. Sci. 123 (1994) 18-25
26. Ferrer I., Pineda M., Tallada M., Oliver B., Russi A., Oller L., Noboa R., Zujar M.J., and Alcantara S. Abnormal local-circuit neurons in epilepsia partialis continua associated with focal cortical dysplasia. Acta Neuropathol. 83 (1992) 647-652
27. Ferrier C.H., Aronica E., Leijten F.S.S., Spliet W.G.M., van Huffelen A.C., van Rijen P.C., and Binnie C. Histology-related electrocorticographic discharge patterns in glioneuronal tumours-a comparison with focal cortical dysplasia. Epilepsia 47 (2006) 1477-1486
28. Furtinger S., Bettler B., and Sperk G. Altered expression of GABAB receptors in the hippocampus after kainic-acid-induced seizures in rats. Brain Res. Mol. Brain Res. 113 (2003) 107-115
29. Garbelli R., Munari C., De Biasi S., Vitellaro-Zuccarello L., Galli C., Bramerio M., Mai R., Battaglia G., and Spreafico R. Taylor's cortical dysplasia: a confocal and ultrastructural immunohistochemical study. Brain Pathol. 9 (1999) 445-461
30. Gonzalez-Albo M.C., Elston G.N., and DeFelipe J. The human temporal cortex: characterization of neurons expressing nitric oxide synthase, neuropeptides and calcium-binding proteins, and their glutamate receptor subunit profiles. Cereb. Cortex 11 (2001) 1170-1181
31. Haglund M.M., Berger M.S., Kunkel D.D., Franck J.E., Ghatan S., and Ojemann G.A. Changes in gamma-aminobutyric acid and somatostatin in epileptic cortex associated with low-grade gliomas. J. Neurosurg. 77 (1992) 209-216
32. Hendry S.H., Huntsman M.M., Vinuela A., Mohler H., de Blas A.L., and Jones E.G. GABAA receptor subunit immunoreactivity in primate visual cortex: distribution in macaques and humans and regulation by visual input in adulthood. J. Neurosci. 14 (1994) 2383-2401
33. Ishikawa M., Mizukami K., Iwakiri M., and Asada T. Immunohistochemical and immunoblot analysis of gamma-aminobutyric acid B receptor in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Neurosci. Lett. 383 (2005) 272-277
34. Ishikawa M., Mizukami K., Iwakiri M., Hidaka S., and Asada T. Immunohistochemical and immunoblot study of GABA(A) alpha1 and beta2/3 subunits in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Neurosci. Res. 50 (2004) 77-84
35. Jones-Davis D.M., and Macdonald R.L. GABA(A) receptor function and pharmacology in epilepsy and status epilepticus. Curr. Opin. Pharmacol. 3 (2003) 12-18
36. Kleihues P., and Cavanee W.K. World Health Organization Classification of Tumours. Pathology and Genetics of Tumours of the Nervous System (2000), IARC Press, Lyon
37. Kohling R., Senner V., Paulus W., and Speckmann E.J. Epileptiform activity preferentially arises outside tumor invasion zone in glioma xenotransplants. Neurobiol. Dis. 22 (2006) 64-75
38. Kriegstein A.R., and Noctor S.C. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27 (2004) 392-399
39. Kuhn S.A., van Landeghem F.K., Zacharias R., Farber K., Rappert A., Pavlovic S., Hoffmann A., Nolte C., and Kettenmann H. Microglia express GABA(B) receptors to modulate interleukin release. Mol. Cell. Neurosci. 25 (2004) 312-322
40. Levitt P. Disruption of interneuron development. Epilepsia 46 (2005) 22-28
41. Li S., Park M.S., and Kim M.O. Prenatal alteration and distribution of the GABA(B1) and GABA(B2) receptor subunit mRNAs during rat central nervous system development. Brain Res. Dev. Brain Res. 150 (2004) 141-150
42. Lopez-Bendito G., Lujan R., Shigemoto R., Ganter P., Paulsen O., and Molnar Z. Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb. Cortex 13 (2003) 932-942
43. Magloczky Z., Wittner L., Borhegyi Z., Halasz P., Vajda J., Czirjak S., and Freund T.F. Changes in the distribution and connectivity of interneurons in the epileptic human dentate gyrus. Neuroscience 96 (2000) 7-25
44. Marco P., Sola R.G., Pulido P., Alijarde M.T., Sanchez A., Ramon y Cajal S., and DeFelipe J. Inhibitory neurons in the human epileptogenic temporal neocortex. An immunocytochemical study. Brain 119 (1996) 1327-1347
45. Marco P., Sola R.G., Ramon y Cajal S., and DeFelipe J. Loss of inhibitory synapses on the soma and axon initial segment of pyramidal cells in human epileptic peritumoural neocortex: implications for epilepsy. Brain Res. Bull. 44 (1997) 47-66
46. Marin-Padilla M. Developmental neuropathology and impact of perinatal brain damage. III. Gray matter lesions of the neocortex. J. Neuropathol. Exp. Neurol. 58 (1999) 407-429
47. Mikuni N., Ikeda A., Takahashi J.A., Nozaki K., Miyamoto S., Taki W., Hashimoto N., 2006. A step-by-step resection guided by electrocorticography for nonmalignant brain tumors associated with long-term intractable epilepsy. Epilepsy Behav. [Epub ahead of print].
48. Munoz A., Arellano J.I., and DeFelipe J. GABABR1 receptor protein expression in human mesial temporal cortex: changes in temporal lobe epilepsy. J. Compar. Neurol. 449 (2002) 166-179
49. Munoz A., DeFelipe J., and Jones E.G. Patterns of GABA(B)R1a,b receptor gene expression in monkey and human visual cortex. Cereb. Cortex 11 (2001) 104-113
50. Nishimura T., Schwarzer C., Gasser E., Kato N., Vezzani A., and Sperk G. Altered expression of GABA(A) and GABA(B) receptor subunit mRNAs in the hippocampus after kindling and electrically induced status epilepticus. Neuroscience 134 (2005) 691-704
51. Patrylo P.R., Spencer D.D., and Williamson A. GABA uptake and heterotransport are impaired in the dentate gyrus of epileptic rats and humans with temporal lobe sclerosis. J. Neurophysiol. 85 (2001) 1533-1542
52. Spreafico R., Battaglia G., Arcelli P., Andermann F., Dubeau F., Palmini A., Olivier A., Villemure J.G., Tampieri D., Avanzini G., and Avoli M. Cortical dysplasia: an immunocytochemical study of three patients. Neurology 50 (1998) 27-36
53. Spreafico R., Tassi L., Colombo N., Bramerio M., Galli C., Garbelli R., Ferrario A., Lo Russo G., and Munari C. Inhibitory circuits in human dysplastic tissue. Epilepsia 41 (2000) S168-S173
54. Straessle A., Loup F., Arabadzisz D., Ohning G.V., and Fritschy J.M. Rapid and long-term alterations of hippocampal GABAB receptors in a mouse model of temporal lobe epilepsy. Eur. J. Neurosci. 18 (2003) 2213-2226
55. Strowbridge B.W., Masukawa L.M., Spencer D.D., and Shepherd G.M. Hyperexcitability associated with localizable lesions in epileptic patients. Brain Res. 587 (1992) 158-163
56. Tassi L., Colombo N., Garbelli R., Francione S., Lo Russo G., Mai R., Cardinale F., Cossu M., Ferrario A., Galli C., Bramerio M., Citterio A., and Spreafico R. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. Brain 125 (2002) 1719-1732
57. Thom M., Harding B.N., Lin W.R., Martinian L., Cross H., and Sisodiya S.M. Cajal-Retzius cells, inhibitory interneuronal populations and neuropeptide Y expression in focal cortical dysplasia and microdysgenesis. Acta Neuropathol. 105 (2003) 561-569
58. Thom M., Martinian L., Parnavelas J.G., and Sisodiya S.M. Distribution of cortical interneurons in grey matter heterotopia in patients with epilepsy. Epilepsia 45 (2004) 916-923
59. Van Gelder N.M., Sherwin A.L., and Rasmussen T. Amino acid content of epileptogenic human brain: focal versus surrounding regions. Brain Res. 40 (1972) 385-393
60. van Veelen C.W., Debets R.M., van Huffelen A.C., van Emde Boas W., Binnie C.D., Storm van Leeuwen W., Velis D.N., and van Dieren A. Combined use of subdural and intracerebral electrodes in preoperative evaluation of epilepsy. Neurosurgery 26 (1990) 93-101
61. Wolf H.K., Birkholz T., Wellmer J., Blumcke I., Pietsch T., and Wiestler O.D. Neurochemical profile of glioneuronal lesions from patients with pharmacoresistant focal epilepsies. J. Neuropathol. Exp. Neurol. 54 (1995) 689-697
62. Wolf H.K., Roos D., Blumcke I., Pietsch T., and Wiestler O.D. Perilesional neurochemical changes in focal epilepsies. Acta Neuropathol. 91 (1996) 376-384