Pilocarpine-induced seizure-like activity with increased BNDF and neuropeptide Y expression in organotypic hippocampal slice cultures

Brain Research

Volumn 950, Issue 1-2, 2002, Pages 103-118

  Poulsen, Frantz Rom ^a   Jahnsen, Henrik ^b   Blaabjerg, Morten ^a   Zimmer, Jens ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

In vitro; Neurotrophins; Propidium iodide; Seizure

Indexed keywords

MUSCARINIC AGENT; MUSCARINIC RECEPTOR BLOCKING AGENT; NEUROPEPTIDE Y; PILOCARPINE; PROPIDIUM IODIDE;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL DEATH; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPILEPTIC DISCHARGE; HIPPOCAMPUS; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; SEIZURE; THETA RHYTHM; WESTERN BLOTTING;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; HIPPOCAMPUS; HUMANS; NEUROPEPTIDE Y; ORGAN CULTURE TECHNIQUES; PILOCARPINE; RATS; RATS, WISTAR; SEIZURES;

EID: 0037144218     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(02)03009-3     Document Type: Article

References (79)

1. Bahr B.A., Kessler M., Rivera S., Vanderklish P.W., Hall R.A., Mutneja M.S., Gall C., Hoffman K.B. Stable maintenance of glutamate receptors and other synaptic components in long-term hippocampal slices. Hippocampus. 5:1995;425-439.
2. Baisden R.H., Woodruff M.L., Hoover D.B. Cholinergic and non-cholinergic septo-hippocampal projections: a double-label horseradish peroxidase-acetylcholinesterase study in the rabbit. Brain Res. 290:1984;146-151.
3. Ballarin M., Ernfors P., Lindefors N., Persson H. Hippocampal damage and kainic acid injection induce a rapid increase in mRNA for BDNF and NGF in the rat brain. Exp. Neurol. 114:1991;35-43.
4. Bendotti C., Pende M., Samanin R. Expression of GAP-43 in the granule cells of rat hippocampus after seizure-induced sprouting of mossy fibres: in situ hybridization and immunocytochemical studies. Eur. J. Neurosci. 6:1994;509-515.
5. Binder D.K., Routbort M.J., Ryan T.E., Yancopoulos G.D., McNamara J.O. Selective inhibition of kindling development by intraventricular administration of TrkB receptor body. J. Neurosci. 19:1999;1424-1436.
6. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy: too much of a good thing? Trends Neurosci. 24:2001;47-53.
7. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., Le Gal La Salle G. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience. 89:1999;717-729.
8. Budziszewska B., Siwanowicz J., Leskiewicz M., Jaworska-Feil L., Lason W. Protective effects of neurosteroids against NMDA-induced seizures and lethality in mice. Eur. Neuropsychopharmacol. 8:1998;7-12.
9. Caulfield M.P. Muscarinic receptors-characterization, coupling and function. Pharmacol. Ther. 58:1993;319-379.
10. Cavalheiro E.A., Silva D.F., Turski W.A., Calderazzo-Filho L.S., Bortolotto Z.A., Turski L. The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Brain Res. 465:1987;43-58.
11. Chen L.S., Wong J.G., Banerjee P.K., Snead O.C. 3rd. Kainic acid-induced focal cortical seizure is associated with an increase of synaptophysin immunoreactivity in the cortex. Exp. Neurol. 141:1996;25-31.
12. Cole A.E., Nicoll R.A. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221:1983;1299-1301.
13. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17:1997;2295-2313.
14. Covolan L., Mello L.E. Temporal profile of neuronal injury following pilocarpine or kainic acid-induced status epilepticus. Epilepsy Res. 39:2000;133-152.
15. Croll S.D., Wiegand S.J., Anderson K.D., Lindsay R.M., Nawa H. Regulation of neuropeptides in adult rat forebrain by the neurotrophins BDNF and NGF. Eur. J. Neurosci. 6:1994;1343-1353.
16. Cronin J., Obenhous A., Houser C., Dudek F.E. Electrophysiology of dentate granule cells after kainate-induced synaptic reorganization of mossy fibers. Brain Res. 573:1992;305-310.
17. Dugich-Djordjevic M.M., Tocco G., Willoughby D.A., Najm I., Pasinetti G., Thompson R.F., Baudry M., Lapchak P.A., Hefti F. BDNF mRNA expression in the developing rat brain following kainic acid-induced seizure activity. Neuron. 8:1992;1127-1138.
18. Ernfors P., Bengzon J., Kokaia A., Persson H., Lindvall O. Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron. 7:1991;165-176.
19. Finsen B.R., Tønder N., Augood S., Zimmer J. Somatostatin and neuropeptide Y in organotypic slice cultures of the rat hippocampus: an immunocytochemical and in situ hybridization study. Neuroscience. 47:1992;105-113.
20. Fischer Y., Gähwiler B.H., Thompson S.M. Activation of intrinsic hippocampal theta oscillations by acetylcholine in rat septo-hippocampal cocultures. J. Physiol. 519:1999;405-413.
21. Gähwiler B.H., Dreifuss J.J. Multiple actions of acetylcholine on hippocampal pyramidal cells in organotypic explant cultures. Neuroscience. 7:1982;1243-1256.
22. Gariboldi M., Conti M., Cavaleri D., Samanin R., Vezzani A. Anticonvulsant properties of BIBP3226, a non-peptide selective antagonist at neuropeptide Y Y1 receptors. Eur. J. Neurosci. 10:1998;757-759.
23. Garzon M., de Andres I., Reinoso-Suarez F. Neocortical and hippocampal electrical activities are similar in spontaneous and cholinergic-induced REM sleep. Brain Res. 766:1997;266-270.
24. Gray W.P., Sundstrom L.E. Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res. 790:1998;52-59.
25. Gutierrez R., Heinemann U. Synaptic reorganization in explanted cultures of rat hippocampus. Brain Res. 815:1999;304-316.
26. Hadar E.J., Yang Y., Sayin U., Rutecki P.A. Suppression of pilocarpine-induced ictal oscillations in the hippocampal slice. Epilepsy Res. 49:2002;61-71.
27. Hajos N., Papp E.C., Acsady L., Levey A.I., Freund T.F. Distinct interneuron types express m2 muscarinic receptor immunoreactivity on their dendrites or axon terminals in the hippocampus. Neuroscience. 82:1998;355-376.
28. Humpel C., Wetmore C., Olson L. Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures. Neuroscience. 53:1993;909-918.
29. Isackson P.J., Murray K., Huntsman M., Gall C.M. BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron. 6:1991;937-948.
30. Jankowsky J.L., Patterson P.H. Differential regulation of cytokine expression following pilocarpine-induced seizure. Exp. Neurol. 159:1999;333-346.
31. Jankowsky J.L., Patterson P.H. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 63:2001;125-149.
32. Jensen M.B., Hegelund I.V., Poulsen F.R., Owens T., Zimmer J., Finsen B. Microglial reactivity correlates to the density and the myelination of the anterogradely degenerating axons and terminals following perforant path denervation of the mouse fascia dentata. Neuroscience. 93:1999;507-518.
33. Katoh-Semba R., Takeuchi I.K., Inaguma Y., Ito H., Kato K. Brain-derived neurotrophic factor, nerve growth and neurotrophin-3 selected regions of the rat brain following kainic acid-induced seizure activity. Neurosci. Res. 35:1999;19-29.
34. Khan G.M., Smolders I., Lindekens H., Manil J., Ebinger G., Michotte Y. Effects of diazepam on extracellular brain neurotransmitters in pilocarpine-induced seizures in rats. Eur. J. Pharmacol. 373:1999;153-161.
35. 2+ transients. Proc. Natl. Acad. Sci. USA. 87:1990;4083-4087.
36. Kokaia Z., Metsis M., Kokaia M., Bengzon J., Elmér E., Smith M.-L., Timmusk T., Siesjö B.K., Persson H., Lindvall O. Brain insults in rats induce increased expression of BDNF gene through differential use of multiple promoters. Eur. J. Neurosci. 6:1994;587-596.
37. Konopacki J., MacIver M.B., Bland B.H., Roth S.H. Carbachol-induced EEG 'theta' activity in hippocampal brain slices. Brain Res. 405:1987;196-198.
38. Kornblum H.I., Sankar R., Shin D.H., Wasterlain C.G., Gall C.M. Induction of brain derived neurotrophic factor mRNA by seizures in neonatal and juvenile rat brain. Mol. Brain Res. 44:1997;219-228.
39. Lauterborn J., Berschauer R., Gall C. Cell-specific modulation of basal and seizure-induced neurotrophin expression by adrenalectomy. Neuroscience. 68:1995;363-378.
40. Leung L.S. Generation of theta and gamma rhythms in the hippocampus. Neurosci. Biobehav. Rev. 22:1998;275-290.
41. Linke R., Frotscher M. Development of the rat septohippocampal projection: tracing with DiI and electron microscopy of identified growth cones. J. Comp. Neurol. 332:1993;69-88.
42. Lüthi A., Gähwiler B.H., Gerber U. A slowly inactivating potassium current in CA3 pyramidal cells of rat hippocampus in vitro. J. Neurosci. 16:1996;586-594.
43. Marksteiner J., Ortler M., Bellmann R., Sperk G. Neuropeptide Y biosynthesis is markedly induced in mossy fibers during temporal lobe epilepsy of the rat. Neurosci. Lett. 112:1990;143-148.
44. Marty S., Onteniente B. BDNF and NT-4 differentiate two pathways in the modulation of neuropeptide protein levels in postnatal hippocampal interneurons. Eur. J. Neurosci. 11:1999;1647-1656.
45. Marty S., Carroll P., Cellerino A., Castren E., Staiger V., Thoenen H., Lindholm D. Brain-derived neurotrophic factor promotes the differentiation of various hippocampal nonpyramidal neurons, including Cajal-Retzius cells, in organotypic slice cultures. J. Neurosci. 16:1996;675-687.
46. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia. 34:1993;985-995.
47. Mello L.E., Kohman C.M., Tan A.M., Cavalheiro E.A., Finch D.M. Lack of Fos-like immunoreactivity after spontaneous seizures or reinduction of status epilepticus by pilocarpine in rats. Neurosci. Lett. 208:1996;133-137.
48. Nagao T., Alonso A., Avoli M. Epileptiform activity induced by pilocarpine in the rat hippocampal-entorhinal slice preparation. Neuroscience. 72:1996;399-408.
49. Nawa H., Carnahan J., Gall C. BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: partial disagreement with mRNA levels. Eur. J. Neurosci. 7:1995;1527-1535.
50. Noraberg J., Kristensen B.W., Zimmer J. Markers for neuronal degeneration in organotypic slice cultures. Brain Res. Protoc. 3:1999;278-290.
51. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J. Neurosci. 17:1997;3727-3738.
52. Parent J.M., Janumpalli S., McNamara J.O., Lowenstein D.H. Increased dentate granule cell neurogenesis following amygdala kindling in the adult rat. Neurosci. Lett. 247:1998;9-12.
53. Poulsen F.R., Lagord C., Courty J., Pedersen E.B., Barritault D., Finsen B. Increased synthesis of heparin affin regulatory peptide in the perforant path lesioned mouse hippocampal formation. Exp. Brain Res. 135:2000;319-330.
54. Reibel S., Larmet Y., Le B.T., Carnahan J., Marescaux C., Depaulis A. Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience. 100:2000;777-788.
55. Richards D.A., Morrone L.A., Bowery N.G. Hippocampal extracellular amino acids and EEG spectral analysis in a genetic rat model of absence epilepsy. Neuropharmacology. 39:2000;2433-2441.
56. Rimvall K., Keller F., Waser P.G. Muscarinic receptors in slice cultures of rat brain. Neuropharmacology. 25:1986;221-226.
57. Rocamora N., Palacios J.M., Mengod G. Limbic seizures induce a differential regulation of the expression of nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 in the rat hippocampus. Mol. Brain Res. 13:1992;27-33.
58. Rouse S.T., Levey A.I. Muscarinic acetylcholine receptor immunoreactivity after hippocampal commissural/associational pathway lesions: evidence for multiple presynaptic receptor subtypes. J. Comp. Neurol. 380:1997;382-394.
59. Rouse S.T., Gilmor M.L., Levey A.I. Differential presynaptic and postsynaptic expression of m1-m4 muscarinic acetylcholine receptors at the perforant pathway/granule cell synapse. Neuroscience. 86:1998;221-232.
60. Rouse S.T., Edmunds S.M., Yi H., Gilmor M.L., Levey A.I. Localization of M(2) muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci. Lett. 284:2000;182-186.
61. Routbort M.J., Bausch S.B., McNamara J.O. Seizures, cell death, and mossy fiber sprouting in kainic acid-treated organotypic hippocampal cultures. Neuroscience. 94:1999;755-765.
62. Rutecki P.A., Yang Y. Ictal epileptiform activity in the CA3 region of hippocampal slices produced by pilocarpine. J. Neurophysiol. 79:1998;3019-3029.
63. Sacaan A.I., Schoepp D.D. Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139:1992;77-82.
64. 2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol. 532:2001;205-216.
65. Sanchez R.M., Wang C., Gardner G., Orlando L., Tauck D.L., Rosenberg P.A., Aizenman E., Jensen F.E. Novel role for the NMDA receptor redox modulatory site in the pathophysiology of seizures. J. Neurosci. 20:2000;2409-2417.
66. Scharfman H.E., Goodman J.H., Sollas A.L., Croll S.D. Spontaneous limbic seizures after intrahippocampal infusion of brain-derived neurotrophic factor. Exp. Neurol. 174:2002;201-214.
67. Smialowska M., Bijak M., Sopala M., Tokarski K. Inhibitory effect of NPY on the picrotoxin-induced activity in the hippocampus: a behavioural and electrophysiological study. Neuropeptides. 30:1996;7-12.
68. Smolders I., Van Belle K., Ebinger G., Michotte Y. Hippocampal and cerebellar extracellular amino acids during pilocarpine-induced seizures in freely moving rats. Eur. J. Pharmacol. 319:1997;21-29.
69. Smolders I., Khan G.M., Manil J., Ebinger G., Michotte Y. NMDA receptor-mediated pilocarpine-induced seizures: characterization in freely moving rats by microdialysis. Br. J. Pharmacol. 121:1997;1171-1179.
70. Tønder N., Kragh J., Finsen B.R., Bolwig T.G., Zimmer J. Kindling induces transient changes in neuronal expression of somatostatin, neuropeptide Y, and calbindin in adult rat hippocampus and fascia dentata. Epilepsia. 35:1994;1299-1308.
71. Turski W.A., Cavalheiro E.A., Schwarz M., Czuczwar S.J., Kleinrok Z., Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav. Brain Res. 9:1983;315-335.
72. Vezzani A., Sperk G., Colmers W.F. Neuropeptide Y: emerging evidence for a functional role in seizure modulation. Trends Neurosci. 22:1999;25-30.
73. Vezzani A., Ravizza T., Moneta D., Conti M., Borroni A., Rizzi M., Samanin R., Maj R. Brain-derived neurotrophic factor immunoreactivity in the limbic system of rats after acute seizures and during spontaneous convulsions: temporal evolution of changes as compared to neuropeptide Y. Neuroscience. 90:1999;1445-1461.
74. N. Vibede, D.P.D. Woldbye, Effects of neuropeptide Yergic agonists on kainic acid seizures in mice, Soc. Neurosci. Abstr. (2000) 732.
75. Wess J. Molecular biology of muscarinic acetylcholine receptors. Crit. Rev. Neurobiol. 10:1996;69-99.
76. Wirth M.J., Obst K., Wahle P. NT-4/5 and LIF, but not NT-3 and BDNF, promote NPY mRNA expression in cortical neurons in the absence of spontaneous bioelectrical activity. Eur. J. Neurosci. 10:1998;1457-1464.
77. Woldbye D.P., Madsen T.M., Larsen P.J., Mikkelsen J.D., Bolwig T.G. Neuropeptide Y inhibits hippocampal seizures and wet dog shakes. Brain Res. 737:1996;162-168.
78. Woldbye D.P., Larsen P.J., Mikkelsen J.D., Klemp K., Madsen T.M., Bolwig T.G. Powerful inhibition of kainic acid seizures by neuropeptide Y via Y5-like receptors. Nat. Med. 3:1997;761-764.
79. Yamamoto J. Effects of nicotine, pilocarpine, and tetrahydroaminoacridine on hippocampal theta waves in freely moving rabbits. Eur. J. Pharmacol. 359:1998;133-137.