Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus

Journal of Neuroscience

Volumn 26, Issue 17, 2006, Pages 4701-4713

  Heinrich, Christophe ^a,b   Nitta, Naoki ^c   Flubacher, Armin ^a   Müller, Martin ^a   Fahrner, Alexander ^a   Kirsch, Matthias ^a   Freiman, Thomas ^a   Suzuki, Fumio ^c   Depaulis, Antoine ^b   Frotscher, Michael ^a   Haas, Carola A ^a,d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b INSERM   (France)

^c SHIGA UNIVERSITY   (Japan)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Ammon's horn sclerosis; Cajal retzius cell; Dentate gyrus; Mesio temporal lobe epilepsy; Neuronal migration; Reelin

Indexed keywords

KAINIC ACID; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CR 50; REELIN; UNCLASSIFIED DRUG; NERVE CELL ADHESION MOLECULE; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; CELL DEGENERATION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; DENTATE GYRUS; ELECTROENCEPHALOGRAM; EPILEPSY; EXPERIMENTAL MODEL; GRANULE CELL; HIPPOCAMPAL SCLEROSIS; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; MALE; MESSENGER RNA SYNTHESIS; MICROGLIA; MITOSIS RATE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEIZURE; TEMPORAL LOBE EPILEPSY; ANIMAL; C57BL MOUSE; CELL MOTION; CELL PROLIFERATION; GRANULOCYTE; PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CELL PROLIFERATION; EPILEPSY, TEMPORAL LOBE; EXTRACELLULAR MATRIX PROTEINS; GRANULOCYTES; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; SERINE ENDOPEPTIDASES;

EID: 33646849420     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5516-05.2006     Document Type: Article

References (56)

1. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
2. 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: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 89:717-729.
3. Bouilleret V, Loup F, Kiener T, Marescaux C, Fritschy JM (2000) Early loss of interneurons and delayed subunit-specific changes in GABA(A)-receptor expression in a mouse model of mesial temporal lobe epilepsy. Hippocampus 10:305-324.
4. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
5. Burbach GJ, Hellweg R, Haas CA, del Turco D, Deicke U, Abramowski D, Jucker M, Staufenbiel M, Deller T (2004) Induction of brain-derived neurotrophic factor in plaque-associated glial cells of aged APP23 transgenic mice. J Neurosci 24:2421-2430.
6. Campbell K, Götz M (2002) Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci 25:235-238.
7. Cendes F, Kahane P, Brodie M, Andermann F (2002) The mesio-temporal lobe epilepsy syndrome. In: Epileptic syndromes in infancy, childhood and adolescence (Roger J, Bureau M, Dravet C, Genton P, Tassinari CA, Wolf P, eds), pp 513-530. Eastleigh, UK: John Libbey and Company.
8. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn HG, Aigner L (2005) Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
9. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.
10. D'Arcangelo G, Homayouni R, Keshvara L, Rice DS, Sheldon M, Curran T (1999) Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.
11. Del Rio JA, Heimrich B, Borrell V, Förster E, Drakew A, Alcantara S, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Derer P, Frotscher M, Soriano E (1997) A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70-74.
12. des Portes V, Pinard JM, Billuart P, Vinet MC, Koulakoff A, Carrie A, Gelot A, Dupuis E, Motte J, Berwald-Netter Y, Catala M, Kahn A, Beldjord C, Chelly J (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92:51-61.
13. Drakew A, Deller T, Heimrich B, Gebhardt C, Del Turco D, Tielsch A, Förster E, Herz J, Frotscher M (2002) Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp Neurol 176:12-24.
14. Eksioglu YZ, Scheffer IE, Cardenas P, Knoll J, DiMario F, Ramsby G, Berg M, Kamuro K, Berkovic SF, Duyk GM, Parisis J, Huttenlocher PR, Walsh CA (1996) Periventricular heterotopia: an X-linked dominant locus causing aberrant cerebral cortical development. Neuron 16:77-87.
15. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
16. 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc Natl Acad Sci USA 99:13178-13183.
17. Frotscher M (1998) Cajal-Retzius cells, reelin and the formation of layers. Curr Opin Neurobiol 8:570-575.
18. Frotscher M, Haas CA, Förster E (2003) Reelin controls granule cell migration in the dentate gyrus by acting on the radial scaffold. Cereb Cortex 13:634-640.
19. Gray WP, Sundstrom LE (1998) Kainic acid increases the proliferation of granule cell progenitors in the dentate gyrus of the adult rat. Brain Res 790:52-59.
20. 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.
21. Haas CA, Deller T, Naumann T, Frotscher M (1996) Selective expression of the immediate early gene c-Jun in axotomized rat medial septal neurons is not related to neuronal degeneration. J Neurosci 16:1884-1903.
22. Haas CA, Deller T, Krsnik Z, Tielsch A, Woods A, Frotscher M (2000) Entorhinal cortex lesion does not alter reelin mRNA expression in the dentate gyrus of young and adult rats. Neuroscience 97:25-31.
23. Haas CA, Dudeck O, Kirsch M, Huszka C, Kann G, Pollak S, Zentner J, Frotscher M (2002) Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J Neurosci 22:5797-5802.
24. Hattiangady B, Rao MS, Shetty AK (2004) Chronic temporal lobe epilepsy is associated with severely declined neurogenesis in the adult hippocampus. Neurobiol Dis 17:473-490.
25. Hirotsune S, Takahare T, Sasaki N, Hirosè K, Yoshiki A, Ohashi T, Kusakabe M, Murakami Y, Muramatsu M, Watanabe S, Nakao K, Katsuki M, Hayashizaki Y (1995) The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat Genet 10:77-83.
26. Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
27. Hong SE, Shugart YY, Hung DT, Al Shahwan S, Garnt PE, Hourihane JO'B, Martin NDT, Walsh C (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 26:93-96.
28. Houser CR (1990) Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res 535:195-204.
29. Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal positioning in the developing brain is regulated by mouse disabled-1. Nature 389:733-737.
30. Hüttmann K, Sadgrove M, Wallraff A, Hinterkeuser S, Kirchhoff F, Steinhäuser C, Gray W (2003) Seizures preferentially stimulate proliferation of radial glia-like astrocytes in the adult dentate gyrus: functional and immunocytochemical analysis. Eur J Neurosci 18:2769-2778.
31. Jessberger S, Römer B, Babu H, Kempermann G (2005) Seizures induce proliferation and dispersion of doublecortin-positive hippocampal progenitor cells. Exp Neurol 196:342-351.
32. Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092-1094.
33. Kralic JE, Ledergerber DA, Frischy J-M (2005) Disruption of the neurogenic potential of the dentate gyrus in a mouse model of temporal epilepsy with focal seizures. Eur J Neurosci 22:1916-1927.
34. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318.
35. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033.
36. Lee J, Auyeung WW, Mattson MP (2003) Interactive effects of excitotoxic injury and dietary restriction on microgliosis and neurogenesis in the hippocampus of adult mice. Neuromol Med 4:179-196.
37. Lurton D, El Bahh B, Sundstrom L, Rougier A (1998) Granule cell dispersion is correlated with early epileptic events in human temporal epilepsy. J Neurol Sci 154:133-136.
38. Margerison JH, Corsellis JAN (1966) Epilepsy and the temporal lobe. Brain 89:499-530.
39. Mathern GW, Leiphart JL, De Vera A, Adelson PD, Seki T, Neder L, Leite JP (2002) Seizures decrease postnatal neurogenesis and granule cell development in the human fascia dentata. Epilepsia 43 [Suppl 5]:68-73.
40. Nakajima K, Mikoshiba K, Miyata T, Yamamoto H, Kudo C, Ogawa M (1997) Disruption of hippocampal development in vivo by CR-50 mAb against reelin. Proc Natl Acad Sci USA 94:8196-8201.
41. Ogawa M, Miyata T, Nakanjima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912.
42. Palmini A, Andermann F, Olivier A, Tampieri D, Robitaille Y, Andermann E, Wright G (1991) Focal neuronal migration disorders and intractable partial epilepsy: a study of 30 patients. Ann Neurol 30:741-749.
43. Parent JM, Yu TW. Leibowitz RT, Geschwind DH, Sloviter RS, Lowenstein DH (1997) Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 17:3727-3738.
44. Rakic P, Caviness VS Jr (1995) Cortical development: view from neurological mutants two decades later. Neuron 14:1101-1104.
45. Rao MS, Shetty AK (2004) Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234-246.
46. Riban V, Bouilleret V, Pham-Le BT, Fritschy J-M, Marescaux C, Depaulis A (2002) Evolution of hippocampal epileptic activity during the development of hippocampal sclerosis in a mouse model of temporal lobe epilepsy. Neuroscience 112:101-111.
47. Ringstedt T, Linnarsson S, Wagner J, Lendahl U, Kokaia Z, Arenas E, Ernfors P, Ibanez CF (1998) BDNFregulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron 21:305-315.
48. Scharfman HE, Goodman JH, Sollas AL (2000) Granule-like neurons at the hilar/CA3 pyramidal cell border after status epilepticus and their synchrony with area CA3 pyramdial cells: functional implications of seizureinduced neurogenesis. J Neurosci 20:6144-6158.
49. Schmued LC, Hopkins KJ (2000) Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 28:91-99.
50. Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351-2358.
51. Sheldon M, Rice DS, d'Arcangelo G, Yoneshima H, Nakajima M, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730-733.
52. 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.
53. Tissir F, Goffinet A (2003) Reelin and brain development. Nat Rev Neurosci 4:496-505.
54. Trommsdorff M, Gotthardt T, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689-701.
55. Weiss KH, Johanssen C, Tielsch A, Herz J, Deller T, Frotscher M, Förster E (2003) Malformation of the radial scaffold in the dentate gyrus of reeler mice, scrambler mice and ApoER2/VLDLR-deficient mice. J Comp Neurol 460:56-65.
56. Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117-5125.