Increase in BDNF-mediated TrkB signaling promotes epileptogenesis in a mouse model of mesial temporal lobe epilepsy

Neurobiology of Disease

Volumn 42, Issue 1, 2011, Pages 35-47

  Heinrich, Christophe ^a,g   Lähteinen, Sari ^b   Suzuki, Fumio ^c   Anne Marie, Laharie ^a   Huber, Susanne ^d   Häussler, Ute ^d   Haas, Carola ^d   Larmet, Yves ^e   Castren, Eero ^f   Depaulis, Antoine ^a  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^d UNIVERSITY OF FREIBURG   (Germany)

^e INSERM   (France)

^f UNIVERSITY OF HELSINKI   (Finland)

^g Department of Physiological Genomics ^*  (Germany)

Author keywords

Ammon's horn sclerosis; Dentate gyrus; Granule cell dispersion; Neuronal plasticity; Neurotrophin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; KAINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTOGENESIS; GRANULE CELL; HIPPOCAMPUS; MALE; MESIAL TEMPORAL LOBE EPILEPSY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TEMPORAL LOBE EPILEPSY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; DENTATE GYRUS; DISEASE MODELS, ANIMAL; EPILEPSY; EPILEPSY, TEMPORAL LOBE; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTOR, TRKB; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 79751532232     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.01.001     Document Type: Article

References (62)

1. Antonucci F., Bozzi Y., Caleo M. Intrahippocampal infusion of botulinum neurotoxin E (BoNT/E) reduces spontaneous recurrent seizures in a mouse model of mesial temporal lobe epilepsy. Epilepsia 2009, 50:963-966.
2. Binder D.K., Croll S.D., Gall C.M., Scharfman H.E. BDNF and epilepsy: too much of a good thing?. Trends Neurosci. 2001, 24:47-53.
3. 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. 1999, 19:1424-1436.
4. 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 1999, 89:717-729.
5. Bovolenta R., Zucchini S., Paradiso B., Rodi D., Merigo F., Navarro Mora G., Osculati F., Berto E., Marconi P., Marzola A., Fabene P.F., Simonato M. Hippocampal FGF-2 and BDNF overexpression attenuates epileptogenesis-associated neuroinflammation and reduces spontaneous recurrent seizures. J. Neuroinflammation 2010, 7:81.
6. Cendes F., Kahane P., Brodie M., Andermann F. The mesio-temporal lobe epilepsy syndrome. Epileptic syndromes in infancy, childhood and adolescence 2002, 513-530. John Libbey & Compagny Ltd. J. Roger, M. Bureau, C. Dravet, P. Genton, C.A. Tassinari, P. Wolf (Eds.).
7. Cendes F., Andermann F., Dubeau F., Gloor P., Evans A., Jones-Gotman M., Olivier A., Andermann E., Robitaille Y., Lopes-Cendes I., et al. Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study. Neurology 1993, 43:1083-1087.
8. 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. Brain-derived neurotrophic factor transgenic mice exhibit passive avoidance deficits, increased seizure severity and in vitro hyperexcitability in the hippocampus and entorhinal cortex. Neuroscience 1999, 93:1491-1506.
9. Danzer S.C., Crooks K.R., Lo D.C., McNamara J.O. Increased expression of brain-derived neurotrophic factor induces formation of basal dendrites and axonal branching in dentate granule cells in hippocampal explant cultures. J. Neurosci. 2002, 22:9754-9763.
10. Dugladze T., Vida I., Tort A.B., Gross A., Otahal J., Heinemann U., Kopell N.J., Gloveli T. Impaired hippocampal rhythmogenesis in a mouse model of mesial temporal lobe epilepsy. Proc. Natl Acad. Sci. USA 2007, 104:17530-17535.
11. Eide F.F., Vining E.R., Eide B.L., Zang K., Wang X.Y., Reichardt L.F. Naturally occurring truncated trkB receptors have dominant inhibitory effects on brain-derived neurotrophic factor signaling. J. Neurosci. 1996, 16:3123-3129.
12. Elmer E., Kokaia Z., Kokaia M., Carnahan J., Nawa H., Lindvall O. Dynamic changes of brain-derived neurotrophic factor protein levels in the rat forebrain after single and recurring kindling-induced seizures. Neuroscience 1998, 83:351-362.
13. Engel J. Mesial temporal lobe epilepsy: what have we learned?. Neuroscientist 2001, 7:340-352.
14. Ernfors P., Wetmore C., Olson L., Persson H. Identification of cells in rat brain and peripheral tissues expressing mRNA for members of the nerve growth factor family. Neuron 1990, 5:511-526.
15. Garcia M.L., Garcia V.B., Isackson P.J., Windebank A.J. Long-term alterations in growth factor mRNA expression following seizures. NeuroReport 1997, 8:1445-1449.
16. Haapasalo A., Koponen E., Hoppe E., Wong G., Castren E. Truncated trkB.T1 is dominant negative inhibitor of trkB.TK+-mediated cell survival. Biochem. Biophys. Res. Commun. 2001, 280:1352-1358.
17. Haas C.A., Deller T., Krsnik Z., Tielsch A., Woods A., Frotscher M. Entorhinal cortex lesion does not alter reelin messenger RNA expression in the dentate gyrus of young and adult rats. Neuroscience 2000, 97:25-31.
18. Haas C.A., Dudeck O., Kirsch M., Huszka C., Kann G., Pollak S., Zentner J., Frotscher M. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 2002, 22:5797-5802.
19. He X.P., Kotloski R., Nef S., Luikart B.W., Parada L.F., McNamara J.O. Conditional deletion of TrkB but not BDNF prevents epileptogenesis in the kindling model. Neuron 2004, 43:31-42.
20. Heinrich C., Nitta N., Flubacher A., Muller M., Fahrner A., Kirsch M., Freiman T., Suzuki F., Depaulis A., Frotscher M., Haas C.A. Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 2006, 26:4701-4713.
21. Hofer M., Pagliusi S.R., Hohn A., Leibrock J., Barde Y.A. Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 1990, 9:2459-2464.
22. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990, 535:195-204.
23. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24:677-736.
24. Jankowsky J.L., Patterson P.H. The role of cytokines and growth factors in seizures and their sequelae. Prog. Neurobiol. 2001, 63:125-149.
25. Kafitz K.W., Rose C.R., Thoenen H., Konnerth A. Neurotrophin-evoked rapid excitation through TrkB receptors. Nature 1999, 401:918-921.
26. Kang H., Schuman E.M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995, 267:1658-1662.
27. Kaplan D.R., Miller F.D. Neurotrophin signal transduction in the nervous system. Curr. Opin. Neurobiol. 2000, 10:381-391.
28. Klein R., Conway D., Parada L.F., Barbacid M. The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain. Cell 1990, 61:647-656.
29. Klesse L.J., Parada L.F. Trks: signal transduction and intracellular pathways. Microsc. Res. Tech. 1999, 45:210-216.
30. Kokaia M., Ernfors P., Kokaia Z., Elmer E., Jaenisch R., Lindvall O. Suppressed epileptogenesis in BDNF mutant mice. Exp. Neurol. 1995, 133:215-224.
31. Koponen E., Voikar V., Riekki R., Saarelainen T., Rauramaa T., Rauvala H., Taira T., Castren E. Transgenic mice overexpressing the full-length neurotrophin receptor trkB exhibit increased activation of the trkB-PLC gamma pathway, reduced anxiety, and facilitated learning. Mol. Cell. Neurosci. 2004, 26:166-181.
32. Kralic J.E., Ledergerber D.A., Fritschy J.M. Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal lobe epilepsy with focal seizures. Eur. J. Neurosci. 2005, 22:1916-1927.
33. Lahteinen S., Pitkanen A., Koponen E., Saarelainen T., Castren E. Exacerbated status epilepticus and acute cell loss, but no changes in epileptogenesis, in mice with increased brain-derived neurotrophic factor signaling. Neuroscience 2003, 122:1081-1092.
34. Lahteinen S., Pitkanen A., Saarelainen T., Nissinen J., Koponen E., Castren E. Decreased BDNF signalling in transgenic mice reduces epileptogenesis. Eur. J. Neurosci. 2002, 15:721-734.
35. Larmet Y., Reibel S., Carnahan J., Nawa H., Marescaux C., Depaulis A. Protective effects of brain-derived neurotrophic factor on the development of hippocampal kindling in the rat. NeuroReport 1995, 6:1937-1941.
36. Lee S., Williamson J., Lothman E.W., Szele F.G., Chesselet M.F., Von Hagen S., Sapolsky R.M., Mattson M.P., Christakos S. Early induction of mRNA for calbindin-D28k and BDNF but not NT-3 in rat hippocampus after kainic acid treatment. Brain Res. Mol. Brain Res. 1997, 47:183-194.
37. Levine E.S., Dreyfus C.F., Black I.B., Plummer M.R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc. Natl Acad. Sci. USA 1995, 92:8074-8077.
38. Mathern GW, Babb TL, Armstrong DL (1997) Hippocampal sclerosis. In.
39. Mathern G.W., Babb T.L., Vickrey B.G., Melendez M., Pretorius J.K. The clinical-pathogenic mechanisms of hippocampal neuron loss and surgical outcomes in temporal lobe epilepsy. Brain 1995, 118(Pt 1):105-118.
40. Mathern G.W., Babb T.L., Leite J.P., Pretorius K., Yeoman K.M., Kuhlman P.A. The pathogenic and progressive features of chronic human hippocampal epilepsy. Epilepsy Res. 1996, 26:151-161.
41. Meier R., Haussler U., Aertsen A., Deransart C., Depaulis A., Egert U. Short-term changes in bilateral hippocampal coherence precede epileptiform events. Neuroimage 2007, 38:138-149.
42. Messaoudi E., Bardsen K., Srebro B., Bramham C.R. Acute intrahippocampal infusion of BDNF induces lasting potentiation of synaptic transmission in the rat dentate gyrus. J. Neurophysiol. 1998, 79:496-499.
43. Middlemas D.S., Lindberg R.A., Hunter T. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol. Cell. Biol. 1991, 11:143-153.
44. Nitta N., Heinrich C., Hirai H., Suzuki F. Granule cell dispersion develops without neurogenesis and does not fully depend on astroglial cell generation in a mouse model of temporal lobe epilepsy. Epilepsia 2008, 49:1711-1722.
45. Osehobo P., Adams B., Sazgar M., Xu Y., Racine R.J., Fahnestock M. Brain-derived neurotrophic factor infusion delays amygdala and perforant path kindling without affecting paired-pulse measures of neuronal inhibition in adult rats. Neuroscience 1999, 92:1367-1375.
46. Palma E., Torchia G., Limatola C., Trettel F., Arcella A., Cantore G., Di Gennaro G., Manfredi M., Esposito V., Quarato P.P., Miledi R., Eusebi F. BDNF modulates GABAA receptors microtransplanted from the human epileptic brain to Xenopus oocytes. Proc. Natl Acad. Sci. USA 2005, 102:1667-1672.
47. Paradiso B., Marconi P., Zucchini S., Berto E., Binaschi A., Bozac A., Buzzi A., Mazzuferi M., Magri E., Navarro Mora G., Rodi D., Su T., Volpi I., Zanetti L., Marzola A., Manservigi R., Fabene P.F., Simonato M. Localized delivery of fibroblast growth factor-2 and brain-derived neurotrophic factor reduces spontaneous seizures in an epilepsy model. Proc. Natl Acad. Sci. USA 2009, 106:7191-7196.
48. Patapoutian A., Reichardt L.F. Trk receptors: mediators of neurotrophin action. Curr. Opin. Neurobiol. 2001, 11:272-280.
49. Paxinos G., Franklin K.B.J. The mouse Brain in Stereotaxic Coordinates 2001, Second Edition, Academic Press, New York.
50. Reibel S., Larmet Y., Le B.T., Carnahan J., Marescaux C., Depaulis A. Brain-derived neurotrophic factor delays hippocampal kindling in the rat. Neuroscience 2000, 100:777-788.
51. Riban V., Bouilleret V., Pham-Le B.T., Fritschy J.M., Marescaux C., Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 2002, 112:101-111.
52. 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. Brain Res. Mol. Brain Res. 1992, 13:27-33.
53. Rudge J.S., Mather P.E., Pasnikowski E.M., Cai N., Corcoran T., Acheson A., Anderson K., Lindsay R.M., Wiegand S.J. Endogenous BDNF protein is increased in adult rat hippocampus after a kainic acid induced excitotoxic insult but exogenous BDNF is not neuroprotective. Exp. Neurol. 1998, 149:398-410.
54. Saarelainen T., Vaittinen S., Castren E. trkB-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell. Mol. Neurobiol. 2001, 21:429-435.
55. 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. Transgenic mice overexpressing truncated trkB neurotrophin receptors in neurons show increased susceptibility to cortical injury after focal cerebral ischemia. Mol. Cell. Neurosci. 2000, 16:87-96.
56. Scharfman H.E. Hyperexcitability in combined entorhinal/hippocampal slices of adult rat after exposure to brain-derived neurotrophic factor. J. Neurophysiol. 1997, 78:1082-1095.
57. 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. 2002, 174:201-214.
58. Simonato M., Tongiorgi E., Kokaia M. Angels and demons: neurotrophic factors and epilepsy. Trends Pharmacol. Sci. 2006, 27:631-638.
59. Suzuki F., Junier M.P., Guilhem D., Sorensen J.C., Onteniente B. Morphogenetic effect of kainate on adult hippocampal neurons associated with a prolonged expression of brain-derived neurotrophic factor. Neuroscience 1995, 64:665-674.
60. Tanaka T., Saito H., Matsuki N. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 1997, 17:2959-2966.
61. Tolwani R.J., Buckmaster P.S., Varma S., Cosgaya J.M., Wu Y., Suri C., Shooter E.M. BDNF overexpression increases dendrite complexity in hippocampal dentate gyrus. Neuroscience 2002, 114:795-805.
62. Wetmore C., Olson L., Bean A.J. Regulation of brain-derived neurotrophic factor (BDNF) expression and release from hippocampal neurons is mediated by non-NMDA type glutamate receptors. J. Neurosci. 1994, 14:1688-1700.