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The Journal of Neuroscience, October 1, 1998, 18(19):7779-7799
Regional and Cellular Patterns of reelin mRNA
Expression in the Forebrain of the Developing and Adult Mouse
Soledad
Alcántara1, 2,
Mónica
Ruiz1,
Gabriella
D'Arcangelo3,
Frederic
Ezan2,
Luis
de Lecea4,
Tom
Curran3,
Constantino
Sotelo2, and
Eduardo
Soriano1
1 Department of Animal and Plant Cell Biology, Faculty
of Biology, University of Barcelona, Barcelona 08028, Spain,
2 Institut National de la Santé et de la Recherche
Médicale U-106, Hôpital de la Salpetrière, 75651 Paris, France, 3 Department of Developmental Neurobiology,
St. Jude Children's Research Hospital, Memphis, Tennessee 38105, and
4 Department of Molecular Biology, The Scripps Research
Institute, La Jolla, California 92037
The reelin gene encodes an extracellular protein
that is crucial for neuronal migration in laminated brain regions. To
gain insights into the functions of Reelin, we performed
high-resolution in situ hybridization analyses to
determine the pattern of reelin expression in the
developing forebrain of the mouse. We also performed double-labeling
studies with several markers, including calcium-binding proteins,
GAD65/67, and neuropeptides, to characterize the neuronal subsets that
express reelin transcripts. reelin
expression was detected at embryonic day 10 and later in the forebrain,
with a distribution that is consistent with the prosomeric model of forebrain regionalization. In the diencephalon, expression was restricted to transverse and longitudinal domains that delineated boundaries between neuromeres. During embryogenesis,
reelin was detected in the cerebral cortex in
Cajal-Retzius cells but not in the GABAergic neurons of layer I. At
prenatal stages, reelin was also expressed in the
olfactory bulb, and striatum and in restricted nuclei in the ventral
telencephalon, hypothalamus, thalamus, and pretectum. At postnatal
stages, reelin transcripts gradually disappeared from
Cajal-Retzius cells, at the same time as they appeared in subsets of
GABAergic neurons distributed throughout neocortical and hippocampal
layers. In other telencephalic and diencephalic regions,
reelin expression decreased steadily during the
postnatal period. In the adult, there was prominent expression in the
olfactory bulb and cerebral cortex, where it was restricted to subsets
of GABAergic interneurons that co-expressed calbindin, calretinin,
neuropeptide Y, and somatostatin. This complex pattern of cellular and
regional expression is consistent with Reelin having multiple roles in
brain development and adult brain function.
Key words:
in situ hybridization; neural development; corticogenesis; neuronal migration; prosomeric subdivisions; Cajal-Retzius cells; GABAergic interneurons
Copyright © 1998 Society for Neuroscience 0270-6474/98/18197779-21$05.00/0
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G. Meyer, J. P. Schaaps, L. Moreau, and A. M. Goffinet
Embryonic and Early Fetal Development of the Human Neocortex
J. Neurosci.,
March 1, 2000;
20(5):
1858 - 1868.
[Abstract]
[Full Text]
[PDF]
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N. R. Smalheiser, E. Costa, A. Guidotti, F. Impagnatiello, J. Auta, P. Lacor, V. Kriho, and G. D. Pappas
Expression of reelin in adult mammalian blood, liver, pituitary pars intermedia, and adrenal chromaffin cells
PNAS,
February 1, 2000;
97(3):
1281 - 1286.
[Abstract]
[Full Text]
[PDF]
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A. Mallamaci, S. Mercurio, L. Muzio, C. Cecchi, C. L. Pardini, P. Gruss, and E. Boncinelli
The Lack of Emx2 Causes Impairment of Reelin Signaling and Defects of Neuronal Migration in the Developing Cerebral Cortex
J. Neurosci.,
February 1, 2000;
20(3):
1109 - 1118.
[Abstract]
[Full Text]
[PDF]
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M. Barallobre, J. Del Rio, S Alcantara, V Borrell, F Aguado, M Ruiz, M. Carmona, M Martin, M Fabre, R Yuste, et al.
Aberrant development of hippocampal circuits and altered neural activity in netrin 1-deficient mice
Development,
January 11, 2000;
127(22):
4797 - 4810.
[Abstract]
[PDF]
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S Alcantara, M Ruiz, F De Castro, E Soriano, and C Sotelo
Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system
Development,
January 4, 2000;
127(7):
1359 - 1372.
[Abstract]
[PDF]
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G. Meyer, A. M. Goffinet, and A. Fairen
Feature Article: What is a Cajal-Retzius cell? A Reassessment of a Classical Cell Type Based on Recent Observations in the Developing Neocortex
Cereb Cortex,
December 1, 1999;
9(8):
765 - 775.
[Full Text]
[PDF]
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D. S. Rice and T. Curran
Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS
Genes & Dev.,
November 1, 1999;
13(21):
2758 - 2773.
[Full Text]
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F. Aboitiz
Feature Article: Evolution of Isocortical Organization. A Tentative Scenario Including Roles of Reelin, p35/cdk5 and the Subplate Zone
Cereb Cortex,
October 1, 1999;
9(7):
655 - 661.
[Abstract]
[Full Text]
[PDF]
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A. A. Lavdas, M. Grigoriou, V. Pachnis, and J. G. Parnavelas
The Medial Ganglionic Eminence Gives Rise to a Population of Early Neurons in the Developing Cerebral Cortex
J. Neurosci.,
September 15, 1999;
19(18):
7881 - 7888.
[Abstract]
[Full Text]
[PDF]
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M. Alvarez-Dolado, M. Ruiz, J. A. Del Rio, S. Alcantara, F. Burgaya, M. Sheldon, K. Nakajima, J. Bernal, B. W. Howell, T. Curran, et al.
Thyroid Hormone Regulates reelin and dab1 Expression During Brain Development
J. Neurosci.,
August 15, 1999;
19(16):
6979 - 6993.
[Abstract]
[Full Text]
[PDF]
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C. Pesold, W. S. Liu, A. Guidotti, E. Costa, and H. J. Caruncho
Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression
PNAS,
March 16, 1999;
96(6):
3217 - 3222.
[Abstract]
[Full Text]
[PDF]
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B. W. Howell, T. M. Herrick, and J. A. Cooper
Reelin-induced tryosine phosphorylation of Disabled 1 during neuronal positioning
Genes & Dev.,
March 15, 1999;
13(6):
643 - 648.
[Abstract]
[Full Text]
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Y Feinstein, V Borrell, C Garcia, T Burstyn-Cohen, V Tzarfaty, A Frumkin, A Nose, H Okamoto, S Higashijima, E Soriano, et al.
F-spondin and mindin: two structurally and functionally related genes expressed in the hippocampus that promote outgrowth of embryonic hippocampal neurons
Development,
January 8, 1999;
126(16):
3637 - 3648.
[Abstract]
[PDF]
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M. A. Rodriguez, C. Pesold, W. S. Liu, V. Kriho, A. Guidotti, G. D. Pappas, and E. Costa
Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex
PNAS,
March 28, 2000;
97(7):
3550 - 3555.
[Abstract]
[Full Text]
[PDF]
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