Advertisement

Ultrastructural Localization of Reelin

  • Rosalinda C. Roberts
  • Emma Perez-Costas

Different chapters of the present book provide background about the molecular, genetic, and biochemical features of the reelin gene, its transcript, and final protein forms. It is not, therefore, our intention to provide an extensive background about the features of the reelin gene and protein, but to emphasize some relevant features that will be helpful for a better understanding of the data reviewed in the present chapter.

Keywords

Dendritic Spine Rough Endoplasmic Reticulum Postsynaptic Density Ultrastructural Localization Axon Initial Segment 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abraham, H., Perez-Garcia, C. G., and Meyer, G. (2004). p73 and reelin in Cajal-Retzius cells of the developing human hippocampal formation. Cereb. Cortex 14:484-495.CrossRefPubMedGoogle Scholar
  2. Akbarian, S., Kim, J. J., Potkin, S. G., Hetrick, W. P., Bunney, W. E., Jr., and Jones, E. G. (1996). Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients. Arch. Gen. Psychiatry 53:425-436.PubMedGoogle 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. 17:7779-7799.Google Scholar
  4. Ballmaier, M., Zoli, M., Leo, G., Agnati, L. F., and Spano, P. (2002). Preferential alterations in the mesolimbic dopamine pathway of heterozygous reeler mice: an emerging animal-based model of schizophrenia. Eur. J. Neurosci. 15:1197-1205.CrossRefPubMedGoogle Scholar
  5. Beffert, U., Weeber, E. J., Durudas, A., Quiu, 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
  6. 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
  7. 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
  8. Borrell, V., Del Rio, J. A., Alcantara, S., Derer, M., Martinez, A., D’Arcangelo, G., Nakajima, K., Mikoshiba, K., Derer, P., Curran, T., and Soriano, E. (1999). Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J. Neurosci. 19:1345-1358.PubMedGoogle Scholar
  9. Candal, E. M., Caruncho, H. J., Sueiro, C., Anadon, R., and Rodriguez-Moldes, I. (2005). Reelin expression in the retina and optic tectum of developing common brown trout. Brain Res. Dev. Brain Res. 154:187-197.CrossRefGoogle Scholar
  10. Caruncho, H. J., Dopeso-Reyes, I. G., Loza, M. I., and Rodriguez, M. A. (2004). GABA, reelin, and the neurodevelopmental hypothesis of schizophrenia. Crit. Rev. Neurobiol. 16:25-32.CrossRefPubMedGoogle Scholar
  11. Chen, Y., Beffert, U., Ertunc, M., Tanq, T. S., Kavalali, E. T., Bezprovanny, I., and Herz, J. (2005). Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci. 25: 8209-8216.CrossRefPubMedGoogle Scholar
  12. 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
  13. D’Arcangelo, G., and Curran, T. (1998). Reeler: new tales on an old mutant mouse. BioEssays 20:235-244.CrossRefPubMedGoogle Scholar
  14. 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
  15. DeFelipe, J., Alonso-Nanclares, L., and Arellano, J. I. (2002). Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31:299-316.CrossRefPubMedGoogle Scholar
  16. 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
  17. Del Rio, J. A., Heimrich, B., Borrell, V., Forster, E., Drakew, A., Alcantara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M., and Soriano, E. (1997). A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70-74.CrossRefPubMedGoogle Scholar
  18. Derer, P., Derer, M., and Goffinet, A. M. (2001). Axonal secretion of reelin by Cajal-Retzius cells: evidence from comparison of normal and RelnOrl mutant mice. J. Comp. Neurol. 440:136-143.CrossRefPubMedGoogle Scholar
  19. 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. 7:157-164.CrossRefPubMedGoogle Scholar
  20. Eastwood, S. L., and Harrison, P. J. (2003). Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and mor-phologic aspects of the neurodevelopmental hypothesis. Mol. Psychiatry 8:821-831.CrossRefGoogle Scholar
  21. 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
  22. Fatemi, S. H., Kroll, J. L., and Stary, J. M. (2001). Altered levels of reelin and its isoforms in schizophrenia and mood disorders. Neuroreport 12:3209-3215.CrossRefPubMedGoogle Scholar
  23. Fatemi, S. H., Stary, J. M., and Egan, E. A. (2002). Reduced blood levels of reelin as a vulnerabil-ity factor in pathophysiology of autistic disorder. Cell. Mol. Neurobiol. 22:139-152.CrossRefPubMedGoogle Scholar
  24. Fatemi, S. H., Snow, A. V., Stary, J. M., Araghi-Niknam, M., Reutiman, T. J., Lee, S., Brooks, A. I., and Pearce D. A. (2005). Reelin signaling is impaired in autism. Biol. Psychiatry 57:777-787.CrossRefPubMedGoogle Scholar
  25. Forster, E., Kaltschmidt, C., Deng, J., Cremer, H., Deller, T., and Frotscher, M. (1998). Lamina-specific cell adhesion on living slices of hippocampus. Development 125:3399-3410.PubMedGoogle Scholar
  26. Glantz, L. A., and Lewis, D. A. (2000). Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry 57:65-73.CrossRefPubMedGoogle Scholar
  27. Goffinet, A. M., Bar, I., Bernier, B., Trujillo, C., Raynaud, A., and Meyer, G. (1999). Reelin expression during embryonic brain development in lazertidian lizards. J. Comp. Neurol. 414:533-550.CrossRefPubMedGoogle Scholar
  28. Guidotti, A., Auta, J., Davis, J. M., DiGiorgi-Generini, V., Dwivedi, Y., Grayson, D. R., Impagnatiello, F., Pandey, G. N., Pesold, C., Sharma, R. F., Uzunov, D. P., and Costa, E. (2000). Decreased reelin and glutamic acid decarboxylase 67 (GAD67) expression in schizo-phrenia and bipolar disorders. Arch. Gen. Psychiatry 57:1061-1069.CrossRefPubMedGoogle Scholar
  29. Herz, J., and Chen, Y. (2006). Reelin, lipoprotein receptors and synaptic plasticity. Nature Rev. Neurosci. 7:850-859.Google Scholar
  30. Hong, S. E., Shugart, Y. Y., Huang, D. T., Shahwan, S. A., Grant, P. E., Hourihane, J. O., Martin, N. D., and Walsh, C. A. (2000). Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nature Genet. 26:93-96.CrossRefPubMedGoogle Scholar
  31. Ikeda, Y., and Terashima, T. (1997). Expression of reelin, the gene responsible for the reeler muta-tion, in embryonic development and adulthood in the mouse. Dev. Dyn. 210:157-172.CrossRefPubMedGoogle Scholar
  32. Impagnatiello, F., Guidotti, A., Pesold, C., Dwivedi, Y., Caruncho, H. J., Pisu, M. G., Uzunov, D. P., Smalheiser, N. R., Davis, J. M., Pandey, G. N., Pappas, G. D., Tueting, P., Sharma, R. P., and Costa, E. (1998). A decrease of reelin expression as a putative vulnerability factor in schizo-phrenia. Proc. Natl. Acad. Sci. USA 95:15718-15723.CrossRefPubMedGoogle Scholar
  33. Kirkpatrick, B., Conley, R. C., Kakoyannis, A., Reep, R. L., and Roberts, R. C. (1999). Interstitial cells of the white matter in the inferior parietal cortex in schizophrenia: An unbiased cell-counting study. Synapse 34:95-102.CrossRefPubMedGoogle Scholar
  34. Kirkpatrick, B., Messias, N. C., Conley, R. R., and Roberts, R. C. (2003). Interstitial cells of the white matter in the dorsolateral prefrontal cortex in deficit and nondeficit schizophrenia. J. Nerv. Ment. Dis. 191:563-567.CrossRefPubMedGoogle Scholar
  35. Kubasak, M. D., Brooks, R., Chen, S., Villeda, S. A., and Phelps, P. E. (2004). Developmental distribution of reelin-positive cells and their secreted production in the rodent spinal cord. J. Comp. Neurol. 468:165-178.CrossRefPubMedGoogle Scholar
  36. Lacor, P. N., Grayson, D. R., Auta, J., Sugaya, I., Costa, E., and Guidotti, A. (2000). Reelin secre-tion from glutamatergic neurons in culture is independent from neurotransmitter regulation. Proc. Natl. Acad. Sci. USA 97:3556-3561.CrossRefPubMedGoogle Scholar
  37. Lambert de Rouvroit, C., and Goffinet A. M. (1998). The reeler mouse as a model of brain devel-opment. Adv. Anat. Embryol. 150:1-106.Google Scholar
  38. Martinez-Cerdeno, V., and Clasca, F. (2002). Reelin immunoreactivity in the adult neocortex: a comparative study in rodents, carnivores and non-human primates. Brain Res. Bull. 57:485-488.Google Scholar
  39. 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. Cereb. Cortex 12:1298-1311.CrossRefPubMedGoogle Scholar
  40. 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 pathways. J. Comp. Neurol. 463:92-116.CrossRefPubMedGoogle Scholar
  41. 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
  42. Meyer, G., Perez-Garcia, 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
  43. Miyata, T., Nakajima, K., Mikoshiba, K., and Ogawa, M. (1997). Regulation of Purkinje cell alignment by reelin as revealed with CR-50 antibody. J. Neurosci. 17:3599-3609.PubMedGoogle Scholar
  44. Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., and D’Arcangelo, G. (2004). Reelin pro-motes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41:71-84.CrossRefPubMedGoogle Scholar
  45. Ohshima, T., Ogawa, M., Veeranna, Hirasawa, M., Longenecker, G., Ishiguro, K., Pant, H. C., Brady, R.O., Kulkarni, A. B., and Mikoshiba, K. (2001). Synergistic contributions of cyclin-dependent kinase 5/p35 and reelin/Dab 1 to the positioning of cortical neurons in the develop-ing mouse brain. Proc. Natl. Acad. Sci. USA 98:2764-2769.CrossRefPubMedGoogle Scholar
  46. Ohshima, T., Ogawa, M., Takeuchi, K., Takahashi, S., Kulkarni, A. B., and Mikoshiba, K. (2002). Cyclin-dependent kinase 57p35 contributes synergistically with reelin/dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. J. Neurosci. 22:4036-4044.PubMedGoogle Scholar
  47. 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 electron microscopy. J. Neurocytol. 30:413-425.CrossRefPubMedGoogle Scholar
  48. Pappas, G. D., Kriho, V., Liu, W. S., Tremolizzo, L., Lugli, G., and Larson, J. (2003). Immunocytochemical localization of reelin in the olfactory bulb of the heterozygous reeler mouse: an animal model for schizophrenia. Neurobiol. Res. 25:819-830.Google Scholar
  49. Perez-Costas, E. (2002). Expresion y distribucion de reelina en el sistema nervioso central de la lamprea. Doctoral thesis. University of Santiago de Compostela, Spain.Google Scholar
  50. Perez-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
  51. Perez-Costas, E., Melendez-Ferro, M., Perez-Garcia, 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
  52. Perez-Garcia, C. G., Gonzalez-Delgado, F. J., Suarez-Sola, M. L., Castro-Fuentes, R., Martin-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
  53. 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
  54. 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 γ-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. USA 95:3221-3226.CrossRefPubMedGoogle Scholar
  55. Pesold, C., Liu, W. S., Guidotti, A., Costa, E., and Caruncho, H. J. (1999). Cortical bitufted, hori-zontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. Proc. Natl. Acad. Sci. USA 96:3127-3222.CrossRefGoogle Scholar
  56. Peters, A. (2002). Examining neocortical circuits: some background and facts. J. Neurocytol. 31:183-193.CrossRefPubMedGoogle Scholar
  57. Phelps, P. E., Rich, R., Dupuy-Davies, S., Rios, Y., and Wong, T. (2002). Evidence for a cell-specific action of reelin in the spinal cord. Dev. Biol. 244:180-198.CrossRefPubMedGoogle Scholar
  58. Qiu, S., Korwek, K. M., Pratt-Davis, A. R., Peters, M., Bergman, M. Y., and Weeber, E. J. (2006). Cognitive disruption and altered hippocampus synaptic function in reelin haploinsufficient mice. Neurobiol. Learn. Memory 85:228-242.CrossRefGoogle Scholar
  59. Rakic, P. (1978). Neuronal migration and contact guidance in the primate telencephalon. Postgrad. Med. J. 1:25-40.Google Scholar
  60. Rakic, P., and Sidman, R. L. (1968). Supravital DNA synthesis in the developing human and mouse brain. J. Neuropathol. Exp. Neurol. 27:246-276.CrossRefPubMedGoogle Scholar
  61. 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
  62. 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
  63. Rice, D. S., and Curran, T. (2001). Role of reelin signalling pathway in central nervous system development. Annu. Rev. Neurosci. 24:1005-1039.CrossRefPubMedGoogle Scholar
  64. 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
  65. Roberts, R.C., Conley, R., Kung, L., Peretti, F. J., and Chute, D. J. (1996). Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study. Neuroreport 7:1214-1218.PubMedCrossRefGoogle Scholar
  66. Roberts, R. C., Xu, L., Roche, J. K., and Kirkpatrick, B. (2005). Ultrastructural localization of reelin in the cortex in postmortem human brain. J. Comp. Neurol. 482:294-308.CrossRefPubMedGoogle Scholar
  67. 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 brain. Proc. Natl. Acad. Sci. USA 97:3550-3555.CrossRefPubMedGoogle Scholar
  68. Rodriguez, 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. 45:279-288.CrossRefGoogle Scholar
  69. 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
  70. Tissir, F., and Goffinet, A. M. (2003). Reelin and brain development. Nature Rev. Neurosci. 4:496-505.Google Scholar
  71. 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
  72. Tueting, P., Costa, E., Dwivedi, Y., Guidotti, A., Impagnatiello, F., Manev, R., and Pesold, C. (1999). The phenotypic characteristics of heterozygous reeler mouse. Neuroreport 10:1329-1334.CrossRefPubMedGoogle Scholar
  73. 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
  74. Yabut, O., Renfro, A., Niu, S., Swann, J. W., Marin, O., and D’Arcangelo, G. (2007). Abnormal laminar position and dendrite development of interneurons in the reeler forebrain. Brain Res. 1140:75-83.CrossRefPubMedGoogle Scholar
  75. Yip, J., Yip, Y. P., Nakajima, K., and Capriotti, C. (2000). Reelin controls position of autonomic neurons in the spinal cord. Proc. Natl. Acad. Sci. USA 97:8612-8616.CrossRefPubMedGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Rosalinda C. Roberts
    • 1
  • Emma Perez-Costas
    • 1
  1. 1.Department of Psychiatry and Behavioral NeurobiologyUniversity of Alabama at Birmingham, SPARKS Center (SC 865D)Birmingham

Personalised recommendations