 |
Previous Article | Next Article 
The Journal of Neuroscience, June 1, 1999, 19(11):4449-4461
Glutamate Acting at NMDA Receptors Stimulates Embryonic Cortical
Neuronal Migration
Toby N.
Behar1, 2,
Catherine A.
Scott1,
Carolyn L.
Greene1,
Xiling
Wen1,
Susan V.
Smith1,
Dragan
Maric1,
Qi-Ying
Liu1,
Carol A.
Colton2, and
Jeffery L.
Barker1
1 Laboratory of Neurophysiology, National Institute of
Neurological Disorders and Stroke, National Institutes of Health,
Bethesda, Maryland 20892, and 2 Department of Physiology
and Biophysics, Georgetown University School of Medicine, Georgetown
University, Washington DC 20007
During cortical development, embryonic neurons migrate from
germinal zones near the ventricle into the cortical plate, where they
organize into layers. Mechanisms that direct neuronal migration may
include molecules that act as chemoattractants. In rats, GABA, which
localizes near the target destination for migrating cortical neurons,
stimulates embryonic neuronal migration in vitro. In mice, glutamate is highly localized near the target destinations for
migrating cortical neurons. Glutamate-induced migration of murine
embryonic cortical cells was evaluated in cell dissociates and cortical
slice cultures. In dissociates, the chemotropic effects of glutamate
were 10-fold greater than the effects of GABA, demonstrating that for
murine cortical cells, glutamate is a more potent chemoattractant than
GABA. Thus, cortical chemoattractants appear to differ between species.
Micromolar glutamate stimulated neuronal chemotaxis that was mimicked
by µM NMDA but not by other ionotropic glutamate receptor
agonists (AMPA, kainate, quisqualate). Responding cells were primarily
derived from immature cortical regions [ventricular zone
(vz)/subventricular zone (svz)]. Bromodeoxyuridine (BrdU) pulse
labeling of cortical slices cultured in NMDA antagonists (µM MK801 or APV) revealed that antagonist exposure
blocked the migration of BrdU-positive cells from the vz/svz
into the cortical plate. PCR confirmed the presence of NMDA receptor
expression in vz/svz cells, whereas electrophysiology and
Ca2+ imaging demonstrated that vz/svz cells
exhibited physiological responses to NMDA. These studies indicate that,
in mice, glutamate may serve as a chemoattractant for neurons in the
developing cortex, signaling cells to migrate into the cortical plate
via NMDA receptor activation.
Key words:
mouse; chemotaxis; cortex; development; slice; chemoattractant
Copyright © 1999 Society for Neuroscience 0270-6474/99/19114449-13$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
X. Liu, K. Hashimoto-Torii, M. Torii, T. F. Haydar, and P. Rakic
The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone
PNAS,
August 19, 2008;
105(33):
11802 - 11807.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. G. Forde and P. J. Lea
Glutamate in plants: metabolism, regulation, and signalling
J. Exp. Bot.,
July 1, 2007;
58(9):
2339 - 2358.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent and A. Represa
Neurotransmitters and Brain Maturation: Early Paracrine Actions of GABA and Glutamate Modulate Neuronal Migration
Neuroscientist,
June 1, 2007;
13(3):
268 - 279.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Cancedda, H. Fiumelli, K. Chen, and M.-m. Poo
Excitatory GABA Action Is Essential for Morphological Maturation of Cortical Neurons In Vivo
J. Neurosci.,
May 9, 2007;
27(19):
5224 - 5235.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. S. Novgorodov, M. El-Alwani, J. Bielawski, L. M. Obeid, and T. I. Gudz
Activation of sphingosine-1-phosphate receptor S1P5 inhibits oligodendrocyte progenitor migration
FASEB J,
May 1, 2007;
21(7):
1503 - 1514.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Heck, W. Kilb, P. Reiprich, H. Kubota, T. Furukawa, A. Fukuda, and H. J. Luhmann
GABA-A Receptors Regulate Neocortical Neuronal Migration In Vitro and In Vivo
Cereb Cortex,
January 1, 2007;
17(1):
138 - 148.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. R. Matsugami, K. Tanemura, M. Mieda, R. Nakatomi, K. Yamada, T. Kondo, M. Ogawa, K. Obata, M. Watanabe, T. Hashikawa, et al.
From the Cover: Indispensability of the glutamate transporters GLAST and GLT1 to brain development
PNAS,
August 8, 2006;
103(32):
12161 - 12166.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent, I. Jorquera, Y. Ben-Ari, L. Aniksztejn, and A. Represa
Glutamate acting on AMPA but not NMDA receptors modulates the migration of hippocampal interneurons.
J. Neurosci.,
May 31, 2006;
26(22):
5901 - 5909.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Alcantara, E. Pozas, C. F. Ibanez, and E. Soriano
BDNF-modulated Spatial Organization of Cajal-Retzius and GABAergic Neurons in the Marginal Zone Plays a Role in the Development of Cortical Organization
Cereb Cortex,
April 1, 2006;
16(4):
487 - 499.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-C. Platel, S. Boisseau, A. Dupuis, J. Brocard, A. Poupard, M. Savasta, M. Villaz, and M. Albrieux
Na+ channel-mediated Ca2+ entry leads to glutamate secretion in mouse neocortical preplate
PNAS,
December 27, 2005;
102(52):
19174 - 19179.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. J. Moody and M. M. Bosma
Ion Channel Development, Spontaneous Activity, and Activity-Dependent Development in Nerve and Muscle Cells
Physiol Rev,
July 1, 2005;
85(3):
883 - 941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-B. Manent, M. Demarque, I. Jorquera, C. Pellegrino, Y. Ben-Ari, L. Aniksztejn, and A. Represa
A Noncanonical Release of GABA and Glutamate Modulates Neuronal Migration
J. Neurosci.,
May 11, 2005;
25(19):
4755 - 4765.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Reiprich, W. Kilb, and H. J. Luhmann
Neonatal NMDA Receptor Blockade Disturbs Neuronal Migration in Rat Somatosensory Cortex In Vivo
Cereb Cortex,
March 1, 2005;
15(3):
349 - 358.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Lee, G. Q. Butcher, K. R. Hoyt, S. Impey, and K. Obrietan
Activity-Dependent Neuroprotection and cAMP Response Element-Binding Protein (CREB): Kinase Coupling, Stimulus Intensity, and Temporal Regulation of CREB Phosphorylation at Serine 133
J. Neurosci.,
February 2, 2005;
25(5):
1137 - 1148.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. M. Adams, J. C. de Rivero Vaccari, and R. A. Corriveau
Pronounced Cell Death in the Absence of NMDA Receptors in the Developing Somatosensory Thalamus
J. Neurosci.,
October 20, 2004;
24(42):
9441 - 9450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. B. Sinclair, A. Sorour, M. Martineau, C. J. Harrison, W. A. Mitchell, E. O'Neill, and L. Foroni
A Fluorescence in Situ Hybridization Map of 6q Deletions in Acute Lymphocytic Leukemia: Identification and Analysis of a Candidate Tumor Suppressor Gene
Cancer Res.,
June 15, 2004;
64(12):
4089 - 4098.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. E. Crandall, H. E. Hackett, S. A. Tobet, B. E. Kosofsky, and P. G. Bhide
Cocaine Exposure Decreases GABA Neuron Migration from the Ganglionic Eminence to the Cerebral Cortex in Embryonic Mice
Cereb Cortex,
June 1, 2004;
14(6):
665 - 675.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Moya and M. Valdeolmillos
Polarized Increase of Calcium and Nucleokinesis in Tangentially Migrating Neurons
Cereb Cortex,
June 1, 2004;
14(6):
610 - 618.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. M. Rodier
Environmental Causes of Central Nervous System Maldevelopment
Pediatrics,
April 1, 2004;
113(4/S1):
1076 - 1083.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Zhang, L. Vutskits, V. Calaora, P. Durbec, and J. Z. Kiss
A role for the polysialic acid - neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells
J. Cell Sci.,
January 1, 2004;
117(1):
93 - 103.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Serge, L. Fourgeaud, A. Hemar, and D. Choquet
Active surface transport of metabotropic glutamate receptors through binding to microtubules and actin flow
J. Cell Sci.,
December 15, 2003;
116(24):
5015 - 5022.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Lopez-Bendito, R. Lujan, R. Shigemoto, P. Ganter, O. Paulsen, and Z. Molnar
Blockade of GABAB Receptors Alters the Tangential Migration of Cortical Neurons
Cereb Cortex,
September 1, 2003;
13(9):
932 - 942.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-H. Chan and H. H Yeh
Enhanced GABAA receptor-mediated activity following activation of NMDA receptors in Cajal-Retzius cells in the developing mouse neocortex
J. Physiol.,
July 1, 2003;
550(1):
103 - 111.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Rakic
Developmental and Evolutionary Adaptations of Cortical Radial Glia
Cereb Cortex,
June 1, 2003;
13(6):
541 - 549.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. C. Luk, T. E. Kennedy, and A. F. Sadikot
Glutamate Promotes Proliferation of Striatal Neuronal Progenitors by an NMDA Receptor-Mediated Mechanism
J. Neurosci.,
March 15, 2003;
23(6):
2239 - 2250.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.M. Soria and M. Valdeolmillos
Receptor-activated Calcium Signals in Tangentially Migrating Cortical Cells
Cereb Cortex,
August 1, 2002;
12(8):
831 - 839.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. A. Haberny, M. G. Paule, A. C. Scallet, F. D. Sistare, D. S. Lester, J. P. Hanig, and W. Slikker Jr.
Ontogeny of the N-Methyl-D-Aspartate (NMDA) Receptor System and Susceptibility to Neurotoxicity
Toxicol. Sci.,
July 1, 2002;
68(1):
9 - 17.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. N. Behar, S. V. Smith, R. T. Kennedy, J. M. Mckenzie, I. Maric, and J. L. Barker
GABAB Receptors Mediate Motility Signals for Migrating Embryonic Cortical Cells
Cereb Cortex,
August 1, 2001;
11(8):
744 - 753.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Rzeski, L. Turski, and C. Ikonomidou
Glutamate antagonists limit tumor growth
PNAS,
April 25, 2001;
(2001)
91113598.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
S. X. Simonian and A. E. Herbison
Differing, Spatially Restricted Roles of Ionotropic Glutamate Receptors in Regulating the Migration of GnRH Neurons during Embryogenesis
J. Neurosci.,
February 1, 2001;
21(3):
934 - 943.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. F. Haydar, F. Wang, M. L. Schwartz, and P. Rakic
Differential Modulation of Proliferation in the Neocortical Ventricular and Subventricular Zones
J. Neurosci.,
August 1, 2000;
20(15):
5764 - 5774.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Metin, J.-P. Denizot, and N. Ropert
Intermediate Zone Cells Express Calcium-Permeable AMPA Receptors and Establish Close Contact with Growing Axons
J. Neurosci.,
January 15, 2000;
20(2):
696 - 708.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Rzeski, L. Turski, and C. Ikonomidou
From the Cover: Glutamate antagonists limit tumor growth
PNAS,
May 22, 2001;
98(11):
6372 - 6377.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|