Comparative Anatomy and Evolutionary Roles of Reelin

  • Gundela Meyer

The reelin gene maps to mouse chromosome 5 and human chromosome 7q22 (DeSilva et al., 1997; Royaux et al., 1997). The mouse reelin gene has a large size, about 450kb, principally due to the presence of some very large introns. It is composed of 65 exons, 51 of which encode the eight reelin repeats. At the 3′-terminal portion of the gene, alternative splicing involves the inclusion of a hexanucleotide AGTAAG encoding amino acids Val-Ser, which create a potential phosphorylation site. This sequence is flanked by two introns and considered a bona fide exon (exon 64) (Royaux et al., 1997). The hexanucleotide sequence is evolutionarily conserved, because it is observed in the same relative location in the turtle and lizard cDNA, while the similar sequence AATAAG is present in chick (Lambert de Rouvrait et al., 1999). An alternative, polyadenylated product corresponds to the alternative exon 63a, expressed in the embryonic mouse brain, that codes for a truncated protein lacking the C-terminal region. This alternative mRNA represents between 10 and 25% of total reelin message in the embryonic mouse brain and is most abundant in Cajal-Retzius neurons of the cerebral cortex and hippocampus and in granule cells of the cerebellum; highly similar sequences are also found in human and rat. While reelin mRNA containing the microexon 64 is the major form in the brain of mouse, rat, man, turtle, and lizard, reelin transcripts in liver and kidney lack the hexanucleotide (Lambert de Rouvrait et al., 1999).


Entorhinal Cortex Comparative Anatomy Lateral Cortex Gestational Week Evolutionary Role 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abraham, H., and Meyer, G. (2003). Reelin-expressing neurons in the postnatal and adult human hippocampal formation. Hippocampus 13: 715-727.CrossRefPubMedGoogle Scholar
  2. Abraham, H., Perez-Garcia, C. G., and Meyer, G. (2004). p73 and reelin in Cajal-Retzius cells of the developing human hippocampal formation. Cerebral Cortex 14:484-495.CrossRefPubMedGoogle Scholar
  3. Alcantara, S., Ruiz, M., D’Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C., and Soriano E. (1998). Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18:7779-7799.PubMedGoogle Scholar
  4. Bar, I., Lambert de Rouvroit, C., and Goffinet, A. M. (2000). The evolution of cortical develop-ment. An hypothesis based on the role of the reelin signaling pathway. Trends Neurosci. 23:633-638.CrossRefPubMedGoogle Scholar
  5. Bar, I., Tissir, F., Lambert de Rouvroit, C., De Backer, O., and Goffinet, A. M. (2003). The gene encoding disabled-1 (DAB1), the intracellular adaptor of the reelin pathway, reveals unusual complexity in human and mouse. J. Biol. Chem. 278:5802-5812.CrossRefPubMedGoogle Scholar
  6. Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W. P., Adelmann, G., Frotscher, M., Hammer, R. E., and Herz, J. (2005). Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47:567-579.CrossRefPubMedGoogle Scholar
  7. Beffert, U., Durudas, A., Weeber, E. J., Stolt, P. C., Giehl, K. M., Sweatt, J. D., Hammer, R. E., and Herz, J. (2006). Functional dissection of reelin signaling by site-directed disruption of disabled-1 adaptor binding to apolipoprotein E receptor 2: distinct roles in development and synaptic plasticity. J. Neurosci. 26:2041-2052.CrossRefPubMedGoogle Scholar
  8. Bernier, B., Bar, I., Pieau, C., Lambert de Rouvroit, C., and Goffinet, A. M. (1999). Reelin mRNA expression during embryonic brain development in the turtle Emys orbicularis. J. Comp. Neurol. 413:463-479.CrossRefPubMedGoogle Scholar
  9. Bernier, B., Bar, I., D’Arcangelo, G., Curran, T., and Goffinet, A. M. (2000). Reelin mRNA expression during embryonic brain development in the chick. J. Comp. Neurol. 422:448-463.CrossRefPubMedGoogle Scholar
  10. Bielle, F., Griveau, A., Narboux-Neme, N., Vigneau, S., Sigrist, M., Arber, S., Wassef, M., and Pierani, A. (2005). Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nature Neurosci. 8:1002-1012.CrossRefPubMedGoogle Scholar
  11. Botella-Lopez, A., Burgaya, F., Gavin, R., Garcia-Ayllon, M. S., Gomez-Tortosa, E., Pena-Casanova, J., Urena, J. M., Del Rio, J. A., Blesa, R., Soriano, E., and Saez-Valero, J. (2006). Reelin expression and glycosylation patterns are altered in Alzheimer’s disease. Proc. Natl. Acad. Sci. USA 103:5573-5578.CrossRefPubMedGoogle Scholar
  12. Braak, H., and Braak, E. (1992). The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci. Res. 15:6-31.CrossRefPubMedGoogle Scholar
  13. Cabrera-Socorro, A., Hernandez-Acosta, N. C., Gonzalez-Gomez, M., and Meyer, G. (2007). Comparative aspects of p73 and reelin expression in Cajal-Retzius cells and the cortical hem in lizard, mouse and human. Brain Res. 1132:59-70.CrossRefPubMedGoogle Scholar
  14. Ceranik, K., Deng, J., Heimrich, B., Lubke, J., Zhao, S., Forster, E., and Frotscher, M. (1999). Hippocampal Cajal-Retzius cells project to the entorhinal cortex: retrograde tracing and intra-cellular labelling studies. Eur. J. Neurosci. 11:4278-4290.CrossRefPubMedGoogle Scholar
  15. Chen, M. L., Chen, S. Y., Huang, C. H., and Chen, C. H. (2002). Identification of a single nucle-otide polymorphism at the 5 promoter region of human reelin gene and association study with schizophrenia. Mol. Psychiatry 7:447-448.CrossRefPubMedGoogle Scholar
  16. Chen, Y., Sharma, R. P., Costa, R. H., Costa, E., and Grayson, D. R. (2002). On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res. 30:2930-2939.CrossRefPubMedGoogle Scholar
  17. Chen, Y., Beffert, U., Ertunc, M., Tang, T. S., Kavalali, E. T., Bezprozvanny, I., and Herz, J. (2005). Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci. 25:8209-8216.CrossRefPubMedGoogle Scholar
  18. Chin, J., Massaro, C. M., Palop, J. J., Thwin, M. T., Yu, G. Q., Bien-Ly, N., Bender, A., and Mucke, L. (2007). Reelin depletion in the entorhinal cortex of human amyloid precursor protein trans-genic mice and humans with Alzheimer’s disease. J. Neurosci. 27:2727-2733.CrossRefPubMedGoogle Scholar
  19. Costagli, A., Kapsimali, M., Wilson, S. W., and Mione, M. (2002). Conserved and divergent patterns of reelin expression in the zebrafish central nervous system. J. Comp. Neurol. 450:73-93.CrossRefPubMedGoogle Scholar
  20. Costagli, A., Felice, B., Guffanti, A., Wilson, S. W., and Mione, M. (2006). Identification of alter-natively spliced dab1 isoforms in zebrafish. Dev.Genes Evol. 216:291-299.CrossRefPubMedGoogle Scholar
  21. D’Arcangelo G., Miao, G. G., Chen, S. C., Soares, H. D., Morgan, J. I., and Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719-723.CrossRefPubMedGoogle Scholar
  22. D’Arcangelo, G., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., and Curran, T. (1997). Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci. 17:23-31.PubMedGoogle Scholar
  23. de Bergeyck, V., Naerhuyzen, B., Goffinet, A. M., and Lambert de Rouvroit, C. (1998). A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice. J. Neurosci. Methods 82:17-24.CrossRefPubMedGoogle Scholar
  24. Deguchi, K., Inoue, K., Avila, W. E., Lopez-Terrada, D., Antalffy, B. A., Quattrocchi, C. C., Sheldon, M., Mikoshiba, K., D’Arcangelo, G., and Armstrong, D. L. (2003). Reelin and disa-bled-1 expression in developing and mature human cortical neurons. J. Neuropathol. Exp. Neurol. 62:676-684.PubMedGoogle Scholar
  25. Derer, P., and Derer, M. (1990). Cajal-Retzius cell ontogenesis and death in mouse brain visual-ized with horseradish peroxidase and electron microscopy. Neuroscience 36:839-856.CrossRefPubMedGoogle Scholar
  26. Derer, P., Derer, M., and Goffinet, A. (2001). Axonal secretion of reelin by Cajal-Retzius cells: evidence from comparison of normal and Reln(Orl) mutant mice. J. Comp. Neurol. 440:136-143.CrossRefPubMedGoogle Scholar
  27. DeSilva, U., D’Arcangelo, G., Braden, V. V., Chen, J., Miao, G. G., Curran, T., and Green, E. D. (1997). The human reelin gene: isolation, sequencing, and mapping on chromosome 7. Genome Res. 199:157-164.CrossRefGoogle Scholar
  28. Drakew, A., Frotscher, M., Deller, T., Ogawa, M., and Heimrich, B. (1998). Developmental distri-bution of a reeler gene-related antigen in the rat hippocampal formation visualized by CR-50 immunocytochemistry. Neuroscience 82:1079-1086.CrossRefPubMedGoogle Scholar
  29. Eastwood, S. L., and Harrison, P. J. (2006). Cellular basis of reduced cortical reelin expression in schizophrenia. Am. J. Psychiatry 163:540-542.CrossRefPubMedGoogle Scholar
  30. Fatemi, S. H., Emamian, E. S., Kist, D., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A., Sheikh, S., and Bailey, K. (1999). Defective corticogenesis and reduction in reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol. Psychiatry 4:145-154.CrossRefPubMedGoogle Scholar
  31. Fatemi, S. H., Earle, J. A., and McMenomy, T. (2000). Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol. Psychiatry 5:654-663.CrossRefPubMedGoogle Scholar
  32. Gertler, F. B., Bennett, R. L., Clark, M. J., and Hoffmann, F. M. (1989). Drosophila abl tyrosine kinase in embryonic CNS axons: a role in axonogenesis is revealed through dosage-sensitive interactions with disabled. Cell 58:103-113.CrossRefPubMedGoogle Scholar
  33. Goffinet, A. M., Bar, I., Bernier, B., Trujillo, C., Raynaud, A., and Meyer, G. (1999). Reelin expression during embryonic brain development in lacertilian lizards. J. Comp. Neurol. 414:533-550.CrossRefPubMedGoogle Scholar
  34. Gomez-Isla, T., Price, J. L., McKeel, D. W., Jr., Morris, J. C., Growdon, J. H., and Hyman, B. T. (1996). Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer’s disease. J. Neurosci. 16:4491-4500.PubMedGoogle Scholar
  35. Hevner, R. F., Neogi, T., Englund, C., Daza, R. A., and Fink, A. (2003). Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res. Dev. Brain Res. 141:39-53.CrossRefGoogle Scholar
  36. Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., and Herz, J. (1999). Direct binding of reelin to VLDL receptor and ApoE receptor 2 induces tyro-sine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.CrossRefPubMedGoogle Scholar
  37. Howell, B. W., Herrick, T. M., and Cooper, J. A. (1999a). Reelin-induced tryosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13:643-648.CrossRefPubMedGoogle Scholar
  38. Howell, B. W., Lanier, L. M., Frank, R., Gertler, F. B., and Cooper, J. A. (1999b). The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glyco-proteins and to phospholipids. Mol. Cell Biol.19:5179-5188.PubMedGoogle Scholar
  39. Jellinger, K., Braak, H., Braak, E., and Fischer, P. (1991). Alzheimer lesions in the entorhinal region and isocortex in Parkinson’s and Alzheimer’s diseases. Ann. N.Y. Acad. Sci. 640:203-209.PubMedGoogle Scholar
  40. Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., Lambert de Rouvroit, C., and Goffinet, A. M. (2004). The central fragment of reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci. 24:514-521.CrossRefPubMedGoogle Scholar
  41. Keshvara, L., Benhayon, D., Magdaleno, S., and Curran, T. (2001). Identification of reelin-induced sites of tyrosyl phosphorylation on disabled 1. J. Biol. Chem. 276:16008-16014.CrossRefPubMedGoogle Scholar
  42. Lambert de Rouvroit, C., and Goffinet, A. M. (1998). The reeler mouse as a model of brain devel-opment. Adv. Anat. Embryol.Cell Biol. 50:1-106.Google Scholar
  43. Lambert de Rouvroit, C., Bernier, B., Royaux, I., de Bergeyck, V., and Goffinet, A. M. (1999). Evolutionarily conserved, alternative splicing of reelin during brain development. Exp. Neurol. 156:229-238.CrossRefPubMedGoogle Scholar
  44. Luque, J. M., Morante-Oria, J., and Fairen, A. (2003). Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development. Brain Res. Dev. Brain Res. 140:195-203.CrossRefGoogle Scholar
  45. Martinez-Cerdeno, V., and Clasca, F. (2002). Reelin immunoreactivity in the adult neocortex: a com-parative study in rodents, carnivores, and non-human primates. Brain Res. Bull. 57:485-488.Google Scholar
  46. Martinez-Cerdeno, V., Galazo, M. J., Cavada, C., and Clasca, F. (2002). Reelin immunoreactivity in the adult primate brain: intracellular localization in projecting and local circuit neurons of the cerebral cortex, hippocampus and subcortical regions. Cerebral Cortex 12:1298-1311.CrossRefPubMedGoogle Scholar
  47. Martinez-Cerdeno, V., Galazo, M. J., and Clasca, F. (2003). Reelin-immunoreactive neurons, axons, and neuropil in the adult ferret brain: evidence for axonal secretion of reelin in long axonal pathways. J. Comp. Neurol. 463:92-116.CrossRefPubMedGoogle Scholar
  48. Meyer, G. (2001). Human neocortical development: the importance of embryonic and early fetal events. Neuroscientist 7:303-314.CrossRefPubMedGoogle Scholar
  49. Meyer, G. (2007). Genetic control of neuronal migrations in human cortical development. Adv. Anat. Embryol. Cell Biol.189:1-111.CrossRefPubMedGoogle Scholar
  50. Meyer, G., and Goffinet, A. M. (1998). Prenatal development of reelin-immunoreactive neurons in the human neocortex. J. Comp. Neurol. 397:29-40.CrossRefPubMedGoogle Scholar
  51. Meyer, G., and González-Hernández, T. (1993). Developmental changes in layer I of the human neocortex during prenatal life: a DiI-tracing and AChE and NADPH-d histochemistry study. J. Comp. Neurol. 338:317-336.CrossRefPubMedGoogle Scholar
  52. Meyer, G., and Wahle, P. (1999). The paleocortical ventricle is the origin of reelin-expressing neurons in the marginal zone of the foetal human neocortex. Eur. J. Neurosci. 11:3937-3944.CrossRefPubMedGoogle Scholar
  53. Meyer, G., Soria, J. M., Martinez-Galan, J. R., Martin-Clemente, B., and Fairen, A. (1998). Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol. 397:493-518.CrossRefPubMedGoogle Scholar
  54. Meyer, G., Goffinet, A. M., and Fairen, A. (1999). What is a Cajal-Retzius cell? A reassessment of a classical cell type based on recent observations in the developing neocortex. Cerebral Cortex 9:765-775.CrossRefPubMedGoogle Scholar
  55. Meyer, G., Pérez-García, C. G., Abraham, H., and Caput, D. (2002). Expression of p73 and reelin in the developing human cortex. J.Neurosci. 22:4973-4986.PubMedGoogle Scholar
  56. Meyer, G., de Rouvroit, C. L., Goffinet, A. M., and Wahle, P. (2003). Disabled-1 mRNA and pro-tein expression in developing human cortex. Eur. J. Neurosci. 17:517-525.CrossRefPubMedGoogle Scholar
  57. Meyer, G., Cabrera-Socorro, A., Pérez-García, C. G., Martínez-Millán, L., Walker, N., and Caput, D. (2004). Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J. Neurosci. 24:9878-9887.CrossRefPubMedGoogle Scholar
  58. Nieuwenhuys, R., and Meek, J. (1990). The telencephalon of actinopterygian fishes. In Jones, G. G., and Peters, A. (Eds.), Cerebral Cortex, Vol. 8A. Plenum Press, New York, pp.31-73.Google Scholar
  59. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., and 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.CrossRefPubMedGoogle Scholar
  60. Pappas, G. D., Kriho, V., and Pesold, C. (2001). Reelin in the extracellular matrix and dendritic spines of the cortex and hippocampus: a comparison between wild type and heterozygous reeler mice by immunoelectron microscopy. J. Neurocytol. 30:413-425.CrossRefPubMedGoogle Scholar
  61. Pérez-Costas, E., Melendez-Ferro, M., Santos, Y., Anadon, R., Rodicio, M. C., and Caruncho, H. J. (2002). Reelin immunoreactivity in the larval sea lamprey brain. J. Chem. Neuroanat. 23:211-221.CrossRefPubMedGoogle Scholar
  62. Pérez-Costas, E., Meléndez-Ferro, M., Pérez-García, C. G., Caruncho, H. J., and Rodicio, M. C. (2004). Reelin immunoreactivity in the adult sea lamprey brain. J. Chem. Neuroanat. 27:7-21.CrossRefPubMedGoogle Scholar
  63. Pérez-García, C. G., González-Delgado, F. J., Suárez-Solá, M. L., Castro-Fuentes, R., Martín-Trujillo, J. M., Ferres-Torres, R., and Meyer, G. (2001). Reelin-immunoreactive neurons in the adult vertebrate pallium. J. Chem. Neuroanat. 21:41-51.CrossRefPubMedGoogle Scholar
  64. Pérez-García, C. G., Tissir, F., Goffinet, A. M., and Meyer, G. (2004). Reelin receptors in develop-ing laminated brain structures of mouse and human. Eur. J. Neurosci. 20:2827-2832.CrossRefPubMedGoogle Scholar
  65. Persico, A. M., D’Agruma, L., Maiorano, N., Totaro, A., Militerni, R., Bravaccio, C., Wassink, T. H., Schneider, C., Melmed, R., Trillo, S., Montecchi, F., Palermo, M., Pascucci, T., Puglisi-Allegra, S., Reichelt, K. L., Conciatori, M., Marino, R., Quattrocchi, C. C., Baldi, A., Zelante, L., Gasparini, P., and Keller, F. (2001). Reelin gene alleles and haplotypes as a factor predisposing to autistic disorder. Mol. Psychiatry 6:150-159.CrossRefPubMedGoogle Scholar
  66. Pesold, C., Impagnatiello, F., Pisu, M. G., Uzunov, D. P., Costa, E., Guidotti, A., and Caruncho, H. J. (1998). Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. USA 95:3221-3226.CrossRefPubMedGoogle Scholar
  67. Pesold, C., Liu, W. S., Guidotti, A., Costa, E., and Caruncho, H. J. (1999). Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. Proc. Natl. Acad. Sci. USA 96:3217-3222.CrossRefPubMedGoogle Scholar
  68. Pollard, K. S., Salama, S. R., Lambert, N., Lambot, M. A., Coppens, S., Pedersen, J. S., Katzman, S., King, B., Onodera, C., Siepel, A., Kern, A. D., Dehay, C., Igel, H., Ares, M., Jr., Vanderhaeghen, P., and Haussler, D. (2006). An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443:167-172.CrossRefPubMedGoogle Scholar
  69. Pozniak, C. D., Radinovic, S., Yang, A., McKeon, F., Kaplan, D. R., and Miller, F. D. (2000). An anti-apoptotic role for the p53 family member, p73, during developmental neuron death. Science 289:304-306.CrossRefPubMedGoogle Scholar
  70. Qiu, S., and Weeber, E. J. (2007). Reelin signaling facilitates maturation of CA1 glutamatergic synapses. J. Neurophysiol. 97:2312-2321.CrossRefPubMedGoogle Scholar
  71. Ramos-Moreno, T., Galazo, M. J., Porrero, C., Martinez-Cerdeno, V., and Clasca, F. (2006). Extracellular matrix molecules and synaptic plasticity: immunomapping of intracellular and secreted reelin in the adult rat brain. Eur. J. Neurosci. 23:401-422.CrossRefPubMedGoogle Scholar
  72. Rice, D. S., and Curran, T. (2001). Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24:1005-1039.CrossRefPubMedGoogle Scholar
  73. Rice, D. S., Sheldon, M., D’Arcangelo, G., Nakajima, K., Goldowitz, D., and Curran, T. (1998). Disabled-1 acts downstream of reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development 125:3719-3729.PubMedGoogle Scholar
  74. Rice, D. S., Nusinowitz, S., Azimi, A. M., Martinez, A., Soriano, E., and Curran, T. (2001). The reelin pathway modulates the structure and function of retinal synaptic circuitry. Neuron 31:929-941.CrossRefPubMedGoogle Scholar
  75. Roberts, R. C., Xu, L., Roche, J. K., and Kirkpatrick, B. (2005). Ultrastructural localization of reelin in the cortex in post-mortem human brain. J. Comp. Neurol. 482:294-308.CrossRefPubMedGoogle Scholar
  76. Rodriguez, M. A., Pesold, C., Liu, W. S., Kriho, V., Guidotti, A., Pappas, G. D., and Costa, E. (2000). Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex. Proc. Natl. Acad. Sci. USA 97:3550-3555.CrossRefPubMedGoogle Scholar
  77. Rodríguez, M. A., Caruncho, H. J., Costa, E., Pesold, C., Liu, W. S., and Guidotti, A. (2002). In Patas monkey, glutamic acid decarboxylase-67 and reelin mRNA coexpression varies in a manner dependent on layers and cortical areas. J. Comp. Neurol. 451:279-288.CrossRefPubMedGoogle Scholar
  78. Royaux, I., Lambert de Rouvroit, C., D’Arcangelo, G., Demirov, D., and Goffinet, A. M. (1997). Genomic organization of the mouse reelin gene. Genomics 46:240-250.CrossRefPubMedGoogle Scholar
  79. Saez-Valero, J., Costell, M., Sjogren, M., Andreasen, N., Blennow, K., and Luque, J. M. (2003). Altered levels of cerebrospinal fluid reelin in frontotemporal dementia and Alzheimer’s dis-ease. J. Neurosci. Res. 72:132-136.CrossRefPubMedGoogle Scholar
  80. Schiffmann, S. N., Bernier, B., and Goffinet, A. M. (1997). Reelin mRNA expression during mouse brain development. Eur. J. Neurosci. 9:1055-1071.CrossRefPubMedGoogle Scholar
  81. Steward, O., and Scoville, S. A. (1976). Cells of origin of entorhinal cortical afferents to the hip-pocampus and fascia dentata of the rat. J. Comp. Neurol. 169:347-370.CrossRefPubMedGoogle Scholar
  82. Tissir, F., and Goffinet, A. M. (2003). Reelin in brain development. Nature Rev. Neurosci. 4:496-505.Google Scholar
  83. Tissir, F., Lambert de Rouvroit, C., and Goffinet, A. M. (2002). The role of reelin in the develop-ment and evolution of the cerebral cortex. Braz. J. Med. Biol. Res. 35:1473-1484.CrossRefPubMedGoogle Scholar
  84. Tissir, F., Lambert de Rouvroit, C., Sire, J. Y., Meyer, G., and Goffinet, A. M. (2003). Reelin expression during embryonic brain development in Crocodylus niloticus. J. Comp. Neurol. 457:250-262.CrossRefPubMedGoogle Scholar
  85. Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., and 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.CrossRefPubMedGoogle Scholar
  86. Ulinski, P. S. (1990). The cerebral cortex of reptiles. In: Jones, E. G., and Peters, A. (Eds.), Cerebral Cortex, Vol. 8A. Plenum Press, New York, pp. 139-215.Google Scholar
  87. van Groen, T., Miettinen, P., and Kadish, I. (2003). The entorhinal cortex of the mouse: organiza-tion of the projection to the hippocampal formation. Hippocampus 13:133-149.CrossRefPubMedGoogle Scholar
  88. Van Hoesen, G. W., and Hyman, B. T. (1990). Hippocampal formation: anatomy and the patterns of pathology in Alzheimer’s disease. Prog. Brain Res. 83:445-457.CrossRefPubMedGoogle Scholar
  89. Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Forster, E., Sweatt, J. D., and Herz, J. (2002). Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277:39944-39952.CrossRefPubMedGoogle Scholar
  90. Willnow, T. E., Nykjaer, A., and Herz, J. (1999). Lipoprotein receptors: new roles for ancient pro-teins. Nature Cell Biol. 1:157-162.CrossRefGoogle Scholar
  91. Witter, M. P., and Groenewegen, H. J. (1984). Laminar origin and septotemporal distribution of entorhinal and perirhinal projections to the hippocampus in the cat. J. Comp. Neurol. 224:371-385.CrossRefPubMedGoogle Scholar
  92. Yang, A., Walker, N., Bronson, R., Kaghad, M., Oosterwegel, M., Bonnin, J., Vagner, C., Bonnet, H., Dikkes, P., Sharpe, A., McKeon, F., and Caput, D. (2000). p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404: 99-103.CrossRefPubMedGoogle Scholar
  93. Yoshida, M., Assimacopoulos, S., Jones, K. R., and Grove, E. A. (2006). Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537-545.CrossRefPubMedGoogle Scholar
  94. Zhao, S., Chai, X., Forster, E., and Frotscher, M. (2004). Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117-5125.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Gundela Meyer
    • 1
  1. 1.Departamento de Anatomía, Facultad de MedicinaUniversidad de La LagunaLa LagunaSpain

Personalised recommendations