Decreased BDNF signalling in transgenic mice reduces epileptogenesis

European Journal of Neuroscience

Volumn 15, Issue 4, 2002, Pages 721-734

  Lähteinen, Sari ^a   Pitkänen, Asla ^a   Saarelainen, Tommi ^a   Nissinen, Jari ^a   Koponen, Eija ^a   Castrén, Eero ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Epilepsy; Hippocampus; Neuropeptide Y; Plasticity; Truncated trkB

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CELL MARKER; KAINIC ACID; NEUROPEPTIDE Y;

ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; DEVELOPMENT; ELECTROENCEPHALOGRAM; EPILEPTIC STATE; EPILEPTOGENESIS; FEMALE; GENOTYPE; IMMUNOCOMPETENT CELL; MALE; MORTALITY; MOSSY FIBER; MOUSE; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; SEIZURE; SPROUT; TRANSGENIC ANIMAL; WILD TYPE;

ACTION POTENTIALS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; DOWN-REGULATION; EPILEPSY; EPILEPSY, TEMPORAL LOBE; EXCITATORY AMINO ACID AGONISTS; FEMALE; GROWTH CONES; MALE; MICE; MICE, TRANSGENIC; MOSSY FIBERS, HIPPOCAMPAL; NERVE DEGENERATION; NEURONAL PLASTICITY; NEUROPEPTIDE Y; RECEPTOR, TRKB; SIGNAL TRANSDUCTION;

EID: 18744409324     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.01897.x     Document Type: Article

References (78)

1. Aloyz, R., Fawcett, J.P., Kaplan, D.R., Murphy, R.A. & Miller, F.D. (1999) Activity-dependent activation of TrkB neurotrophin receptors in the adult CNS. Learn Mem., 6, 216-231.
2. 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.
3. Ben-Ari, Y., Tremblay, E., Riche, D., Ghilini, G. & Naquet, R. (1981) Electrographic, clinical and pathological alterations following systemic administration of kainic acid, bicuculline or pentetrazole: Metabolic mapping using the deoxyglucose method with special reference to the pathology of epilepsy. Neuroscience, 6, 1361-1391.
4. Bender, R., Heimrich, B., Meyer, M. & Frotscher, M. (1998) Hippocampal mossy fiber sprouting is not impaired in brain-derived neurotrophic factor-deficient mice. Exp. Brain Res., 120, 399-402.
5. Biagini, G., Avoli, M., Marcinkiewicz, J. & Marcinkiewicz, M. (2001) Brain-derived neurotrophic factor superinduction parallels anti-epileptic-neuroprotective treatment in the pilocarpine epilepsy model. J. Neurochem., 76, 1814-1822.
6. Binder, D.K., Routbort, M.J., Ryan, T.E., Yancopoulos, G.D. & McNamara, J.O. (1999) Selective inhibition of kindling development by intraventricular administration of TrkB receptor body. J. Neurosci., 19, 1424-1436.
7. Buckmaster, P.S. & Dudek, F.E. (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.
8. Castren, E., Thoenen, H. & Lindholm, D. (1995) Brain-derived neurotrophic factor messenger RNA is expressed in the septum, hypothalamus and in adrenergic brain stem nuclei of adult rat brain and is increased by osmotic stimulation in the paraventricular nucleus. Neuroscience, 64, 71-80.
9. Cavazos, J.E., Golarai, G. & Sutula, T.P. (1991) Mossy fiber synaptic reorganization induced by kindling: Time course of development, progression, and permanence. J. Neurosci., 11, 2795-2803.
10. Croll, S.D., Suri, C., Compton, D.L., Simmons, M.V., Yancopoulos, G.D., Lindsay, R.M., Wiegand, S.J., Rudge, J.S. & Scharfman, H.E. (1999) Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience, 93, 1491-1506.
11. Eide, F.F., Vining, E.R., Eide, B.L., Zang, K., Wang, X.Y. & Reichardt, L.F. (1996) Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signalling. J. Neurosci., 16, 3123-3129.
12. Elmer, E., Kokaia, Z., Kokaia, M., Carnahan, J., Nawa, H. & Lindvall, O. (1998) Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience, 83, 351-362.
13. Elmer, E., Kokaia, M., Kokaia, Z., Ferencz, I. & Lindvall, O. (1996) Delayed kindling development after rapidly recurring seizures: Relation to mossy fiber sprouting and neurotrophin, GAP-43 and dynorphin gene expression. Brain Res., 712, 19-34.
14. Elmer, E., Kokaia, Z., Kokaia, M., Lindvall, O. & McIntyre, D.C. (1997) Mossy fibre sprouting: Evidence against a facilitatory role in epileptogenesis. Neuroreport, 8, 1193-1196.
15. Ernfors, P., Bengzon, J., Kokaia, Z., Persson, H. & Lindvall, O. (1991) Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis. Neuron, 7, 165-176.
16. Fawcett, J.P., Aloyz, R., McLean, J.H., Pareek, S., Miller, F.D., McPherson, P.S. & Murphy, R.A. (1997) Detection of brain-derived neurotrophic factor in a vesicular fraction of brain synaptosomes. J. Biol. Chem., 272, 8837- 8840.
17. Fawcett, J.P., Bamji, S.X., Causing, C.G., Aloyz, R., Ase, A.R., Reader, T.A., McLean, J.H. & Miller, F.D. (1998) Functional evidence that BDNF is an anterograde neuronal trophic factor in the CNS. J. Neurosci., 18, 2808-2821.
18. Ferraro, T.N., Golden, G.T., Smith, G.G. & Berrettini, W.H. (1995) Differential susceptibility to seizures induced by systemic kainic acid treatment in mature DBA/2J and C57BL/6J mice. Epilepsia, 36, 301-307.
19. Frank, L., Ventimiglia, R., Anderson, K., Lindsay, R.M. & Rudge, J.S. (1996) BDNF down-regulates neurotrophin responsiveness, TrkB protein and TrkB mRNA levels in cultured rat hippocampal neurons. Eur. J. Neurosci., 8, 1220-1230.
20. Franklin, K.B. & Paxinos, G. (1997). The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
21. French, J.A., Williamson, P.D., Thadani, V.M., Darcey, T.M., Mattson, R.H., Spencer, S.S. & Spencer, D.D. (1993) Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Annu. Neurol., 34 , 774-780.
22. Gall, C.M. (1993) Seizure-induced changes in neurotrophin expression: Implications for epilepsy. Exp. Neurol., 124, 150-166.
23. Gall, C.M. & Isackson, P.J. (1989) Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science, 245, 758- 761.
24. Gall, C., Lauterborn, J., Isackson, P. & White, J. (1990) Seizures, neuropeptide regulation, and mRNA expression in the hippocampus. Prog. Brain. Res., 83 , 371-390.
25. Haapasalo, A., Koponen, E., Hoppe, E., Wong, G. & Castren, E. (2001) Truncated trkB.T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival. Biochem. Biophys. Res. Commun., 280, 1352-1358.
26. Houser, C.R., Miyashiro, J.E., Swartz, B.E., Walsh, G.O., Rich, J.R. & Delgado-Escueta, A.V. (1990) Altered patterns of dynorphin immunoreactivity suggest mossy fiber reorganisation in human hippocampal epilepsy. J. Neurosci., 10, 267-282.
27. Jutila, L., Immonen, A., Partanen, K., Partanen, J., Mervaala, E., Ylinen, A., Alafuzoff, I., Paljärvi, L., Karkola, K., Vapalahti, M. & Pitkänen, A. (2002) Neurobiology of epileptogenesis in the temporal lobe. Adv. Techn. Standards in Neurosurgery, in press.
28. Kang, H. & Schuman, E.M. (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science, 267, 1658-1662.
29. Klein, R., Conway, D., Parada, L.F. & Barbacid, M. (1990) The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell, 61, 647-656.
30. Knusel, B., Gao, H., Okazaki, T., Yoshida, T., Mori, N., Hefti, F. & Kaplan, D.R. (1997) Ligand-induced down-regulation of Trk messenger RNA, protein and tyrosine phosphorylation in rat cortical neurons. Neuroscience, 78 , 851-862.
31. Knusel, B., Rabin, S.J., Hefti, F. & Kaplan, D.R. (1994) Regulated neurotrophin receptor responsiveness during neuronal migration and early differentiation. J. Neurosci., 14, 1542-1554.
32. Kokaia, M., Ernfors, P., Kokaia, Z., Elmer, E., Jaenisch, R. & Lindvall, O. (1995) Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol., 133, 215-224.
33. Larmet, Y., Reibel, S., Carnahan, J., Nawa, H., Marescaux, C. & Depaulis, A.(1995) Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. Neuroreport, 6, 1937-1941.
34. Levine, E.S., Dreyfus, C.F., Black, I.B. & Plummer, M.R. (1995) Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl. Acad. Sci. USA, 92, 8074-8077.
35. Lewin, G.R. & Barde, Y.A. (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci., 19, 289-317.
36. Lindholm, D., Castren, E., Berzaghi, M., Blochl, A. & Thoenen, H. (1994) Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain - implications for neuronal plasticity. J. Neurobiol., 25, 1362- 1372.
37. Lindvall, O., Kokaia, Z., Bengzon, J., Elmer, E. & Kokaia, M. (1994) Neurotrophins and brain insults. Trends Neurosci., 17, 490-496.
38. Lohof, A.M., Ip, N.Y. & Poo, M.M. (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature, 363, 350-353.
39. Lothman, E.W. & Collins, R.C. (1981) Kainic acid induced limbic seizures: Metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res., 218, 299-318.
40. 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.
41. Mathern, G.W., Babb, T.L., Micevych, P.E., Blanco, C.E. & Pretorius, J.K. (1997) Granule cell mRNA levels for BDNF, NGF, and NT-3 correlate with neuron losses or supragranular mossy fiber sprouting in the chronically damaged and epileptic human hippocampus. Mol. Chem. Neuropathol., 30, 53-76.
42. McAllister, A.K., Katz, L.C. & Lo, D.C. (1999) Neurotrophins and synaptic plasticity. Annu. Rev. Neurosci., 22, 295-318.
43. Middlemas, D.S., Lindberg, R.A. & Hunter, T. (1991) TrkB, a neural receptor protein-tyrosine kinase: Evidence for a full-length and two truncated receptors. Mol. Cell Biol., 11, 143-153.
44. Muller-Schwarze, A.B., Tandon, P., Liu, Z., Yang, Y., Holmes, G.L. & Stafstrom, C.E. (1999) Ketogenic diet reduces spontaneous seizures and mossy fiber sprouting in the kainic acid model. Neuroreport, 10, 1517-1522.
45. Nadler, J.V., Perry, B.W. & Cotman, C.W. (1980a) Selective reinnervation of hippocampal area CA1 and the fascia dentata after destruction of CA3-CA4 afferents with kainic acid. Brain Res., 182, 1-9.
46. Nadler, J.V., Perry, B.W., Gentry, C. & Cotman, C.W. (1980b) Degeneration of hippocampal CA3 pyramidal cells induced by intraventricular kainic acid. J. Comp. Neurol., 192, 333-359.
47. Nawa, H., Carnahan, J. & Gall, C. (1995) BDNF protein measured by a novel enzyme immunoassay in normal brain and after seizure: Partial disagreement with mRNA levels. Eur. J. Neurosci., 7, 1527-1535.
48. Ninkina, N., Adu, J., Fischer, A., Pinon, L.G.P., Buchman, V.L. & Davies, A.M. (1996) Expression and function of TrkB variants in developing sensory neurons. EMBO J., 15, 6385-6393.
49. Nissinen, J., Halonen, T., Koivisto, E. & Pitkänen, A. (2000) A new model of chronic temporal lobe epilepsy induced by electrical stimulation of the amygdala in rat. Epilepsy Res., 38, 177-205.
50. Olofsdotter, K., Lindvall, O. & Asztely, F. (2000) Increased synaptic inhibition in dentate gyrus of mice with reduced levels of endogenous brain-derived neurotrophic factor. Neuroscience, 101, 531-539.
51. Osehobo, P., Adams, B., Sazgar, M., Xu, Y., Racine, R.J. & Fahnestock, M. (1999) Brain-derived neurotrophic factor infusion delays amygdala and perforant path kindling without affecting paired-pulse measures of neuronal inhibition in adult rats. Neuroscience, 92, 1367-1375.
52. Phillips, H.S., Hains, J.M., Laramee, G.R., Rosenthal, A. & Winslow, J.W. (1990) Widespread expression of BDNF but not NT3 by target areas of basal forebrain cholinergic neurons. Science, 250, 290-294.
53. Pitkänen, A., Tuunanen, J. & Halonen, T. (1996) Vigabatrin and carbamazepine have different efficacies in the prevention of status epilepticus induced neuronal damage in the hippocampus and amygdala. Epilepsy Res., 24, 29-45.
54. Qiao, X., Suri, C.G.D.Y., Noebels, J. & Knusel, B. (1997) Absence of mossy fiber sprouting in transgenic mice overexpressing BDNF in the dentate gyrus. Soc. Neurosci. Abstract, 23, 331.
55. Racine, R.J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol., 32, 281-294.
56. Reibel, S., Larmet, Y., Le, B.T., Carnahan, J., Marescaux, C. & Depaulis, A. (2000) Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience, 100, 777-788.
57. Routbort, M.J., Ryan, T.E., Yancopoulos, G.D. & J.O.M. (1997) TrkB-IgG does not inhibit mossy fiber sprouting in an. In Vitro Model. Soc. Neurosci Abstract, 23, 888.
58. Royle, S.J., Collins, F.C., Rupniak, H.T., Barnes, J.C. & Anderson, R. (1999) Behavioural analysis and susceptibility to CNS injury of four inbred strains of mice. Brain Res., 816, 337-349.
59. Saarelainen, T., Lukkarinen, J.A., Koponen, S., Grohn, O.H., Jolkkonen, J., Koponen, E., Haapasalo, A., Alhonen, L., Wong, G., Koistinaho, J., Kauppinen, R.A. & Castren, E. (2000) Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons show increased susceptibility to cortical injury after focal cerebral ischemia. Mol. Cell Neurosci., 16, 87-96.
60. Saarelainen, T., Vaittinen, S. & Castrèn, E. (2001) TrkB receptor activation contributes to the kainate induced increase in BDNF mRNA synthesis. Cell. Mol. Neurobiol., 21 (4), 429-435.
61. Scharfman, H.E. (1997) Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor. J. Neurophysiol., 78, 1082-1095.
62. Scharfman, H.E., Goodman, J.H. & Sollas, A.L. (1999) Actions of brain-derived neurotrophic factor in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. J. Neurosci., 19, 5619-5631.
63. Schauwecker, P.E., Ramirez, J.J. & Steward, O. (2000) Genetic dissection of the signals that induce synaptic reorganization. Exp. Neurol., 161, 139-152.
64. Schauwecker, P.E. & Steward, O. (1997) Genetic determinants of susceptibility to excitotoxic cell death: Implications for gene targeting approaches. Prog. Natl. Acad. Sci., 49, 4103-4108.
65. Schwarzer, C., Sperk, G., Samanin, R., Rizzi, M., Gariboldi, M. & Vezzani, A. (1996) Neuropeptides-immunoreactivity and their mRNA expression in kindling: functional implications for limbic epileptogenesis. Brain Res. Brain Res. Rev., 22, 27-50.
66. Schwob, J.E., Fuller, T., Price, J.L. & Olney, J.W. (1980) Widespread patterns of neuronal damage following systemic or intracerebral injections of kainic acid: A histological study. Neuroscience, 5, 991-1014.
67. Shelton, D.L., Sutherland, J., Gripp, J., Camerato, T., Armanini, M.P., Phillips, H.S., Carroll, K., Spencer, S.D. & Levinson, A.D. (1995) Human trks: Molecular cloning, tissue distribution, and expression of extracellular domain immunoadhesins. J. Neurosci., 15, 477-491.
68. Sloviter, R.S. (1982) A simplified Timm stain procedure compatible with formaldehyde fixation and routine paraffin embedding of rat brain. Brain Res. Bull., 8, 771-774.
69. Sommerfeld, M.T., Schweigreiter, R., Barde, Y.A. & Hoppe, E. (2000) Down-regulation of the neurotrophin receptor TrkB following ligand binding. Evidence for an involvement of the proteasome and differential regulation of TrkA and TrkB. J. Biol. Chem., 275, 8982-8990.
70. Sperk, G. (1994) Kainic acid seizures in rat. Prog. Neurobiol., 42, 1-32.
71. Stafstrom, C.E., Thompson, J.L. & Holmes, G.L. (1992) Kainic acid seizures in the developing brain: Status epilepticus and spontaneous recurrent seizures. Brain Res. Dev. Brain Res., 65, 227-236.
72. Sutula, T., Cascino, G., Cavazos, J., Parada, I. & Ramirez, L. (1989) Mossy fiber synaptic reorganisation in the epileptic human temporal lobe. Annu. Neurol., 26, 321-330.
73. Takahashi, M., Hayashi, S., Kakita, A., Wakabayashi, K., Fukuda, M., Kameyama, S., Tanaka, R., Takahashi, H. & Nawa, H. (1999) Patients with temporal lobe epilepsy show an increase in brain-derived neurotrophic factor protein and its correlation with neuropeptide Y. Brain Res., 818, 579- 582.
74. Takahashi, Y., Tsunashima, K., Sadamatsu, M., Schwarzer, C., Amano, S., Ihara, N., Sasa, M., Kato, N. & Sperk, G. (2000) Altered hippocampal expression of neuropeptide Y, somatostatin, and glutamate decarboxylase in Ihara's epileptic rats and spontaneously epileptic rats. Neurosci. Lett., 287, 105-108.
75. Thoenen, H. (1995) Neurotrophins and neuronal plasticity. Science, 270, 593- 598.
76. Tuunanen, J., Lukasiuk, K., Halonen, T. & Pitkänen, A. (1999) Status epilepticus-induced neuronal damage in the rat amygdaloid complex: Distribution, time-course and mechanisms. Neuroscience, 94, 473-495.
77. Wisden, W. & Morris, B. (1994) In situ hybridisation with synthetic oligonucleotide probes. In Wisden, W. & Morris, B. (eds), In situ Hybridisation Protocols for Neurobiology. Academic Press, London.
78. Zachrisson, O., Mathe, A.A., Stenfors, C. & Lindefors, N. (1995) Limbic effects of repeated electroconvulsive stimulation on neuropeptide Y and somatostatin mRNA expression in the rat brain. Brain Res. Mol. Brain Res., 31 , 71-85.