Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal lobe epilepsy

Hippocampus

Volumn 10, Issue 3, 2000, Pages 305-324

  Bouilleret, Viviane ^a   Loup, Fabienne ^b   Kiener, Tania ^b   Marescaux, Christian ^a   Fritschy, Jean Marc ^b  

^a INSERM   (France)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Calcium binding proteins; Hippocampal sclerosis; Kainic acid; Recurrent seizures; Type 1 GABA transporter

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CALBINDIN; CALRETININ; KAINIC ACID; PARVALBUMIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROL; CONTROLLED STUDY; DENTATE GYRUS; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TEMPORAL LOBE EPILEPSY;

EID: 0033921793     PISSN: 10509631     EISSN: None     Source Type: Journal    
DOI: 10.1002/1098-1063(2000)10:3<305::AID-HIPO11>3.0.CO;2-I     Document Type: Article

References (99)

1. Association for the Study of Animal Behavior. 1993. Guideline for the use of animals in research. Animal Behav 45:209-212.
2. Babb TL, Pretorius JK, Kupfer WR, Crandall PH. 1989. Glutamate decarboxylase-immunoreactive neurons are preserved in human epileptic hippocampus. J Neurosci 9:2562-2574.
3. Babb TL, Pretorius JK, Mello LE, Mathern GW, Levesque MF. 1992. Synaptic reorganizations in epileptic human and rat kainate hippocampus may contribute to feedback and feedforward excitation. Epilepsy Res Suppl 9:193-203.
4. Bekenstein JW, Lothman EW. 1993. Dormancy of inhibitory interneurons in a model of temporal lobe epilepsy. Science 259:97-100.
5. 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.
6. Blasco-Ibanez JM, Freund TF. 1997. Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307-320.
7. Blumcke I, Beck H, Nitsch R, Eickhoff C, Scheffler B, Celio MR, Schramm J, Elger CE, Wolf HK, Wiestler OD. 1996. Preservation of calretinin-immunoreactive neurons in the hippocampus of epilepsy patients with Ammon's horn sclerosis. J Neuropathol Exp Neurol 55:329-341.
8. Blumcke I, Beck H, Suter B, Hoffmann D, Fodish HJ, Wolf HK, Schramm J, Elger CE, Wiestler OD. 1999. An increase of hippocampal calretinin-immunoreactive neurons correlates with early febrile seizures in temporal lobe epilepsy. Acta Neuropathol (Berl) 97:31-39.
9. Borden LA. 1996. GABA transporter heterogeneity: pharmacology and cellular localization. Neurochem Int 29:335-356.
10. Bouilleret V, Ridoux V, Depaulis A, Marescaux C, Nehlig A, Le Gal La Salle G. 1999. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: EEG, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 89:717-729.
11. A receptor subunit expression and function in temporal lobe epilepsy. Nat Med 4:1166-1172.
12. Buckmaster PS, Dudek FE. 1997. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385:385-404.
13. Buhl EH, Otis TS, Mody I. 1996. Zinc-induced collapse of augmented inhibition by GABA in a temporal lobe epilepsy model. Science 271: 369-373.
14. 2+ -permeable AMPA/kainate channels triggers marked intracellular Ca rises and consequent oxygen radical production. J Neurosci 18:7727-7738.
15. Cavalheiro EA, Leite JP, Bortolotto ZA, Turski WA, Ikonomidou C, Turski L. 1991. Long-term effects of pilocarpine in rats: structural damage of the brain triggers kindling and spontaneous recurrent seizures. Epilepsia 32:778-782.
16. Cavazos JE, Das I, Sutula TP. 1994. Neuronal loss induced in limbic pathways by kindling: evidence for induction of hippocampal sclerosis by repeated brief seizures. J Neurosci 14:3106-3121.
17. Celio MR. 1990. Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375-475.
18. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y. 1998. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470.
19. Cronin J, Dudek FE. 1988. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res 474:181-184.
20. Davenport CJ, Brown WJ, Babb TL. 1990. Sprouting of GABAergic and mossy fiber axons in dentate gyrus following intrahippocampal kainate in the rat. Exp Neurol 109:180-190.
21. 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.
22. Dudek FE, Obenaus A, Schweitzer JS, Wuarin JP. 1994. Functional significance of hippocampal plasticity in epileptic brain: electrophysiological changes of the dentate granule cells associated with mossy fiber sprouting. Hippocampus 4:259-265.
23. During MJ, Ryder KM, Spencer DD. 1995. Hippocampal GABA transporter function in temporal-lobe epilepsy. Nature 376:174-177.
24. Engel J. 1993. Update on surgical treatment of the epilepsies: summary of the second Palm Desert Conference on the surgical treatment of the epilepsies. Neurology 43:1612-1617.
25. Engstrom FL, Woodbury DM. 1988. Seizure susceptibility in DBA and C57 mice: the effects of various convulsants. Epilepsia 29:389-395.
26. Esclapez M, Hirsch JC, Khazipov R, Ben-Ari Y, Bernard C. 1997. Operative GABAergic inhibition in hippocampal CA1 pyramidal neurons in experimental epilepsy. Proc Natl Acad Sci USA 94:12151-12156.
27. Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C. 1999. Newly formed excitatory pathways provide a substrate for hyperexcitability in experimental temporal lobe epilepsy. J Comp Neurol 408:449-460.
28. Fisher PD, Sperber EF, Moshe SL. 1998. Hippocampal sclerosis revisited. Brain Dev 20:563-573.
29. Frerking M, Malenka RC, Nicoll RA. 1998. Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1:479-486.
30. Freund TF, Buzsaki G. 1996. Interneurons of the hippocampus. Hippocampus 6:345-470.
31. A-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154-194.
32. A-receptor subunits revealed by antigen-retrieval immunohistochemistry. J Comp Neurol 390:194-210.
33. A-receptors in temporal lobe epilepsy. Neurochem Int 34: 435-445.
34. Fujise N, Liu Y, Hori N, Kosaka T. 1998. Distribution of calretinin immunoreactivity in the mouse dentate gyrus: II. Mossy cells, with special reference to their dorsoventral difference in calretinin immunoreactivity. Neuroscience 82:181-200.
35. Gale K. 1992. GABA and epilepsy: basic concepts from preclinical research. Epilepsia 33 (Suppl. 5):S3-S12.
36. A-receptors containing the α1-subunit to neurochemically distinct subpopulations of hippocampal interneurons. Eur J Neurosci 6:837-853.
37. A receptor function in dentate granule and CA1 neurons. J Neurophysiol 77:1924-1938.
38. Gloor P. 1991. Mesial temporal lobe sclerosis: historical background and an overview from a modern perspective. In: Luders H, editor. Epilepsy surgery. New York: Raven Press, p 689.
39. Guentschev M, Groschup MH, Kordek R, Liberski PP, Budka H. 1998. Severe, early and selective loss of a subpopulation of GABAergic inhibitory neurons in experimental transmissible spongiform encephalopathies. Brain Pathol 8:615-623.
40. Guilhem D, Dreyfus PA, Makiura Y, Suzuki F, Onteniente B. 1996. Short increase of BDNF messenger RNA triggers kainic acid-induced neuronal hypertrophy in adult mice. Neuroscience 72:923-931.
41. Hamani C, Tenorio F, Mendez-Otero R, Mello LEAM. 1999. Loss of NADPH diaphorase-positive neurons in the hippocampal formation of chronic pilocarpine-epileptic rats. Hippocampus 9:303-313.
42. Hashimoto T, Obata K. 1991. Induction of somatostatin by kainic acid in pyramidal and granule cells of the rat hippocampus. Neurosci Res 12:514-527.
43. Houser CR. 1990. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 535:195-204.
44. Houser CR. 1991. GABA neurons in seizure disorders: a review of immunocytochemical studies. Neurochem Res 16:295-308.
45. Houser CR. 1992. Morphological changes in the dentate gyrus in human temporal lobe epilepsy. Epilepsy Res Suppl 7:223-234.
46. Hsu SM, Raine L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577-580.
47. Hu RQ, Koh S, Torgerson T, Cole AJ. 1998. Neuronal stress and injury in C57/BL mice after systemic kainic acid administration. Brain Res 810:229-240.
48. Inoue T, Hirai H, Onteniente B, Suzuki F. 1998. Correlated long-term increase of brain-derived neurotrophic factor and Trk B proteins in enlarged granule cells of mouse hippocampus after kainic acid injection. Neuroscience 86:723-728.
49. A receptor-mediated inhibitory postsynaptic currents in dentate granule cells in epileptic hippocampus. J Neurophysiol 75:1901-1908.
50. A receptor-mediated inhibition by postsynaptic calcium in epileptic hippocampal neurons. Brain Res 810:241-250.
51. 2+-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol (Lond) 485:383-402.
52. Kotti T, Tapiola T, Riekkinen PJ, Miettinen R. 1996. The calretinincontaining mossy cells survive excitotoxic insult in the gerbil dentate gyrus. Comparison of excitotoxicity-induced neuropathological changes in the gerbil and rat. Eur J Neurosci 8:2371-2378.
53. Kurschner VC, Petruzzi RL, Golden GT, Berrettini WH, Ferraro TN. 1998. Kainate and AMPA receptor binding in seizure-prone and seizure-resistant inbred mouse strains. Brain Res 780:1-8.
54. Leite JP, Babb TL, Pretorius JK, Kuhlman PA, Yeoman KM, Mathern GW. 1998. Neuron loss, mossy fiber sprouting, and interictal spikes after intrahippocampal kainate in developing rats. Epilepsy Res 26: 219-231.
55. Leranth C, Ribak CE. 1991. Calcium-binding proteins are concentrated in the CA2 field of the monkey hippocampus: a possible key to this region's resistance to epileptic damage. Exp Brain Res 85:129-136.
56. Leranth C, Szeidemann Z, Hsu M, Buzsaki G. 1996. AMPA receptors in the rat and primate hippocampus - a possible absence of GLUR2/3 subunits in most interneurons. Neuroscience 70:631-652.
57. Loscher W. 1998. New visions in the pharmacology of anticonvulsion. Eur J Pharmacol 342:1-13.
58. A-receptors in the hippocampal formation of temporal lobe epilepsy patients. Soc Neurosci Abstr 23: 816.
59. Magloczky Z, Freund TF. 1993. Selective neuronal death in the contralateral hippocampus following unilateral kainate injections into the CA3 subfield. Neuroscience 56:317-335.
60. Magloczky Z, Freund TF. 1995. Delayed cell death in the contralateral hippocampus following kainate injection into the CA3 subfield. Neuroscience 66:847-860.
61. Makiura Y, Suzuki F, Chevalier E, Onteniente B. 1999. Excitatory granule cells of the dentate gyrus exhibit a double inhibitory neurochemical content after intrahippocampal administration of kainate in adult mice. Exp Neurol 159:73-83.
62. Mangan PS, Rempe DA, Lothman EW. 1995. Changes in inhibitory neurotransmission in the CA1 region and dentate gyrus in a chronic model of temporal lobe epilepsy. J Neurophysiol 74:829-840.
63. Margerison JH, Corsellis JA. 1966. Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 89:499-530.
64. Marksteiner J, Ortler M, Bellmann R, Sperk G. 1990. Neuropeptide Y biosynthesis is markedly induced in mossy fibers during temporal lobe epilepsy of the rat. Neurosci Lett 112:143-148.
65. Mathern GW, Babb TL, Pretorius JK, Leite JP. 1995. Reactive synaptogenesis and neuron densities for neuropeptide Y, somatostatin, and glutamate decarboxylase immunoreactivity in the epileptogenic human fascia dentata. J Neurosci 15:3990-4004.
66. Mathern GW, Mendoza D, Lozada A, Pretorius JK, Kehnes 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.
67. Meldrum B. 1979. Convulsant drugs, anticonvulsants and GABA-mediated neuronal inhibition. In: Krogsgard-Larsen P, Scheell-Kruger J, Kofod H, editors. GABA neurotransmitters. Copenhagen: Munksgaard, p 390-405.
68. Mello L, Cavalheiro EA, Tan AM, Kupfer WR, Pretorius JK, Babb TL, Finch DM. 1993. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34:985-995.
69. A-receptors: from subunits to diverse functions. In: Narahashi T, editor. Ion channels, vol 4, New York: Plenum Press, p 89-113.
70. Nadler JV. 1981. Kainic acid as a tool for the study of temporal lobe epilepsy. Life Sci 29:2031-2042.
71. A receptors underlies potentiation at hippocampal synapses. Nature 395:172-177.
72. Obenaus A, Esclapez M, Houser CR. 1993. Loss of glutamate decarboxylase mRNA-containing neurons in the rat dentate gyrus following pilocarpine-induced seizures. J Neurosci 13:4470-4485.
73. Olsen RW, Avoli M. 1997. GABA and epileptogenesis. Epilepsia 38:399-407.
74. Ribak CE, Tong WMY, Brecha NC. 1996. GABA plasma membrane transporters, GAT-1 and GAT-3, display different distributions in the rat hippocampus. J Comp Neurol 367:595-606.
75. Rice A, Rafiq A, Shapiro SM, Jakoi ER, Coulter DA, DeLorenzo RJ. 1996. Long-lasting reduction of inhibitory function and γ-aminobutyric acid type A receptor subunit mRNA expression in a model of temporal lobe epilepsy. Proc Natl Acad Sci USA 93:9665-9669.
76. Robbins RJ, Brines ML, Kim JH, Adrian T, de Lanerolle NC, Welsh S, Spencer DD. 1992. A selective loss of somatostatin in the hippocampus of patients with temporal lobe epilepsy. Ann Neurol 29:325-332.
77. Royle SJ, Collins FC, Rupniak HT, Barnes JC, Anderson R. 1999. Behavioural analysis and susceptibility to CNS injury of four inbred strains of mice. Brain Res 816:337-349.
78. Schauwecker PE, Steward O. 1997. Genetic determinants of susceptibility to excitotoxic cell death - implications for gene targeting approaches. Proc Natl Acad Sci USA 94:4103-4108.
79. A receptor subunits in the rat hippocampus. II. Altered distribution in kainic acid-induced temporal lobe epilepsy. Neuroscience 80:1001-1017.
80. Scotti AL, Kalt G, Bollag O, Nitsch C. 1997. Parvalbumin disappears from GABAergic CA1 neurons of the gerbil hippocampus with seizure onset while its presence persists in the perforant path. Brain Res 760: 109-117.
81. A receptor function in epileptic human dentate granule cells - comparison to epileptic and control rat. Epilepsy Res 32:114-128.
82. Sloviter RS. 1987. Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73-76.
83. Sloviter RS. 1989. Calcium-binding protein (calbindin-D28k) and parvalbumin immunohistochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183-196.
84. Sloviter RS. 1991 Permanently altered hippocampal structure, excitability, and inhibition after experimental status epilepticus in the rat: the "dormant basket cell" hypothesis and its possible relevance to temporal lobe epilepsy. Hippocampus 1:41-66.
85. Sloviter RS. 1992. Possible functional consequences of synaptic reorganization in the dentate gyrus of kainate-treated rats. Neurosci Lett 137: 91-96.
86. Sloviter RS. 1994a. The functional organization of the hippocampal dentate gyrus and its relevance to the pathogenesis of temporal lobe epilepsy. Ann Neurol 35:640-654.
87. Sloviter RS. 1994b. On the relationship between neuropathology and pathophysiology in the epileptic hippocampus of humans and experimental animals. Hippocampus 4:250-253.
88. Sloviter RS, Sollas AL, Barbaro NM, Laxer KD. 1991. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308: 381-396.
89. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL, Martin DL. 1996. Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373:593-618.
90. Sperk G. 1994. Kainic acid seizures in the rat. Prog Neurobiol 42:1-32.
91. Sutula TP, Cavazos JE, Woodard AR. 1994. Long-term structural and functional alterations induced in the hippocampus by kindling: implications for memory dysfunction and the development of epilepsy. Hippocampus 4:254-258.
92. Suzuki F, Junier MP, Guilhem D, Sorensen JC, Onteniente B. 1995. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience 64:665-674.
93. Suzuki F, Makiura Y, Guilhem D, Sorensen JC, Onteniente B. 1997. Correlated axonal sprouting and dendritic spine formation during kainate-induced neuronal morphogenesis in the dentate gyrus of adult mice. Exp Neurol 145:202-213.
94. Tashiro Y, Chakrabortty S, Drake JM, Hattori T. 1997. Progressive loss of glutamic acid decarboxylase, parvalbumin, and calbindin D28K immunoreactive neurons in the cerebral cortex and hippocampus of adult rat with experimental hydrocephalus. J Neurosurg 86:263-271.
95. Tasker JG, Dudek FE. 1991. Electrophysiology of GABA-mediated synaptic transmission and possible roles in epilepsy. Neurochem Res 16: 251-262.
96. Toth Z, Hollrigel GS, Gores T, Soltesz I. 1997. Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J Neurosci 17:8106-8117.
97. Vezzani A, Civenni G, Rizzi M, Monno A, Messali S, Samanin R. 1994. Enhanced neuropeptide Y release in the hippocampus is associated with chronic seizure susceptibility in kainic acid treated rats. Brain Res 660:138-143.
98. A receptor currents. Neuroreport 6:461-464.
99. Williamson A, Telfeian AE, Spencer DD. 1995. Prolonged GABA responses in dentate granule cells in slices isolated from patients with temporal lobe sclerosis. J Neurophysiol 74:378-387.