Exogenous reelin prevents granule cell dispersion in experimental epilepsy

Experimental Neurology

Volumn 216, Issue 2, 2009, Pages 390-397

  Müller, Martin C ^a   Osswald, Matthias ^a   Tinnes, Stefanie ^a   Häussler, Ute ^a   Jacobi, Anne ^a   Förster, Eckart ^a   Frotscher, Michael ^a   Haas, Carola A ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Ammon's horn sclerosis; apoER2; dab1; Dentate gyrus; Extracellular matrix; Neurogenesis; Neuronal migration; Temporal lobe epilepsy; VLDLR

Indexed keywords

ADAPTOR PROTEIN; APOLIPOPROTEIN E2; KAINIC ACID; LIPOPROTEIN RECEPTOR; REELIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEGENERATION; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; CONTROLLED STUDY; DENTATE GYRUS; EPILEPSY; EXTRACELLULAR MATRIX; GRANULE CELL; HIPPOCAMPUS; HOSPITAL SERVICE; IN SITU HYBRIDIZATION; MALE; MIGRATION; MOUSE; NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; STEM CELL; TEMPORAL LOBE; TEMPORAL LOBE EPILEPSY; WESTERN BLOTTING;

ADAPTOR PROTEIN COMPLEX 1; ANALYSIS OF VARIANCE; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL COUNT; CELL MOVEMENT; DENTATE GYRUS; DISEASE MODELS, ANIMAL; DRUG DELIVERY SYSTEMS; EPILEPSY; EXCITATORY AMINO ACID AGONISTS; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; KAINIC ACID; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURAL INHIBITION; NEURONS; NEUROPROTECTIVE AGENTS; RECEPTORS, LDL; RECEPTORS, LIPOPROTEIN; RNA, MESSENGER; SERINE ENDOPEPTIDASES; TIME FACTORS;

EID: 62049084965     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.12.029     Document Type: Article

References (28)

1. Bock H.H., Jossin Y., Liu P., Förster E., May P., Goffinet A.M., and Herz J. Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. J. Biol. Chem. 278 (2003) 38772-38779
2. Bouilleret V., Ridoux V., Depaulis A., Marescaux C., Nehlig A., and 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
3. Bouilleret V., Loup F., Kiener T., Marescaux C., and Fritschy J.M. Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus 10 (2000) 305-324
4. Carroll P., Gayet O., Feuillet C., Kallenbach S., de Bovis B., Dudley K., and Alonso S. Juxtaposition of CNR protocadherins and reelin expression in the developing spinal cord. Mol. Cell. Neurosci. 17 (2001) 611-623
5. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., and Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995) 719-723
6. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., and Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 24 (1999) 471-479
7. Förster E., Tielsch A., Saum B., Weiss K.H., Johanssen C., Graus-Porta D., Müller U., and Frotscher M. Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13178-13183
8. Förster E., Zhao S., and Frotscher M. Laminating the hippocampus. Nat. Rev., Neurosci. 7 (2006) 259-267
9. Frotscher M., Haas C.A., and Förster E. Reelin controls granule cell migration in the dentate gyrus by acting on the radial glial scaffold. Cereb. Cortex 13 (2003) 634-640
10. Gleeson J.G., and Walsh C.A. Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci. 23 (2000) 352-359
11. Gong C., Wang T.W., Huang H.S., and Parent J.M. Reelin regulates neuronal progenitor migration in intact and epileptic hippocampus. J. Neurosci. 27 (2007) 1803-1811
12. Haas C.A., Dudeck O., Kirsch M., Huszka C., Kann G., Pollak S., Zentner J., and Frotscher M. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 22 (2002) 5797-5802
13. Heinrich C., Nitta N., Flubacher A., Muller M., Fahrner A., Kirsch M., Freiman T., Suzuki F., Depaulis A., Frotscher M., and 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. 26 (2006) 4701-4713
14. Herz J., and Bock H.H. Lipoprotein receptors in the nervous system. Annu. Rev. Biochem. 71 (2002) 405-434
15. Hirotsune S., Takahara T., Sasaki N., Hirose K., Yoshiki A., Ohashi T., Kusakabe M., Murakami Y., Muramatsu M., Watanabe S., Nakao K., Katsuki M., and Hayashizaki Y. The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat. Genet. 10 (1995) 77-83
16. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain. Res. 535 (1990) 195-204
17. Howell B.W., Hawkes R., Soriano P., and Cooper J.A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389 (1997) 733-737
18. Jossin Y., Gui L., and Goffinet A.M. Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J. Neurosci. 27 (2007) 4243-4252
19. Kempermann G., Jessberger S., Steiner B., and Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27 (2004) 447-452
20. Kralic J.E., Ledergerber D.A., and 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. 22 (2005) 1916-1927
21. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 (2004) 71-84
22. Palmini A., Andermann F., Olivier A., Tampieri D., Robitaille Y., Andermann E., and Wright G. Focal neuronal migration disorders and intractable partial epilepsy: a study of 30 patients. Ann. Neurol. 30 (1991) 741-749
23. Rakic P., and Caviness Jr. V.S. Cortical development: view from neurological mutants two decades later. Neuron 14 (1995) 1101-1104
24. Riban V., Bouilleret V., Pham-Le B.T., Fritschy J.-M., Marescaux C., and Depaulis A. Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 112 (2002) 101-111
25. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., Howell B.W., Cooper J.A., Goldowitz D., and Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389 (1997) 730-733
26. Tissir F., and Goffinet A.M. Reelin and brain development. Nat. Rev., Neurosci. 4 (2003) 496-505
27. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., and Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97 (1999) 689-701
28. Zhao S., Chai X., Forster E., and Frotscher M. Reelin is a positional signal for the lamination of dentate granule cells. Development 131 (2004) 5117-5125