 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 15, 3039-3052, Copyright © 1995 by Society for Neuroscience
Maturation-dependent upregulation of growth-promoting molecules in developing cortical plate controls thalamic and cortical neurite growth
R Tuttle, BL Schlaggar, JE Braisted and DD O'Leary
Molecular Neurobiology Laboratory, Salk Institute, La Jolla, California 92037, USA.
We have tested the hypothesis that maturation-dependent changes in the
cortical plate affect the spatiotemporal growth patterns of developing
thalamocortical and corticocortical axonal projections. Given a choice
between alternating lanes of embryonic (E18-19) and neonatal (P0-1) rat
cortical plate membranes, embryonic (E18-19) thalamic and cortical neurites
prefer to extend on neonatal membranes. Thalamic and cortical explants do
extend neurites on uniform carpets of E19 cortical plate membranes, but the
outgrowth is consistently greater on uniform carpets of P1 cortical plate
membranes. These experiments demonstrate a maturation-dependent enhancement
in the ability of cortical plate to support neurite growth from thalamic
and cortical explants. In contrast, retinal and cerebellar neurites, which
do not grow into cortex in vivo, generally grew poorly on these membranes,
suggesting a degree of specificity to the neurite growth response.
Immunohistochemical analysis of developing cortex suggests that several
extracellular matrix (ECM) and cell adhesion molecules are upregulated in
cortical plate. However, immunocharacterization of membrane carpets for
these same ECM and cell adhesion molecules suggests that the growth
preferences of thalamic and cortical neurites in vitro are predominantly
influenced by membrane-anchored, rather than ECM, molecules. Western
analysis of E19 and P1 cortical plate membranes supports this conclusion,
and indicates that the membrane-anchored cell adhesion molecules L1 and
N-CAM are more abundant in the P1 cortical plate membrane preparation.
Experiments in which cortical plate membranes were treated to remove
molecules sensitive to phosphatidylinositol (PI)-specific phospholipase C
demonstrate that neurite growth promoters present in E19 cortical plate
membranes are predominantly PI linked, whereas those present in P1
membranes are predominantly non-PI linked. These findings indicate that the
neurite growth preferences are mediated, at least in part, by an
upregulation of neurite growth-promoting molecules in developing cortical
plate that are not PI linked. Taken together, these findings suggest that a
maturation-dependent upregulation of neurite growth-promoting molecules on
cortical plate cells controls the invasion of the cortical plate by
thalamocortical and corticocortical axons.
This article has been cited by other articles:
|
|
|
|
 
M. C. Manzini, M. S. Ward, Q. Zhang, M. D. Lieberman, and C. A. Mason
The stop signal revised: immature cerebellar granule neurons in the external germinal layer arrest pontine mossy fiber growth.
J. Neurosci.,
May 31, 2006;
26(22):
6040 - 6051.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Leingartner, L. J. Richards, R. H. Dyck, C. Akazawa, and D. D.M. O'Leary
Cloning and Cortical Expression of Rat Emx2 and Adenovirus-mediated Overexpression to Assess its Regulation of Area-specific Targeting of Thalamocortical Axons
Cereb Cortex,
June 1, 2003;
13(6):
648 - 660.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Poskanzer, L. A. Needleman, O. Bozdagi, and G. W. Huntley
N-Cadherin Regulates Ingrowth and Laminar Targeting of Thalamocortical Axons
J. Neurosci.,
March 15, 2003;
23(6):
2294 - 2305.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Mann, C. Peuckert, F. Dehner, R. Zhou, and J. Bolz
Ephrins regulate the formation of terminal axonal arbors during the development of thalamocortical projections
Development,
March 10, 2003;
129(16):
3945 - 3955.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. M. Ughrin, Z. J. Chen, and J. M. Levine
Multiple Regions of the NG2 Proteoglycan Inhibit Neurite Growth and Induce Growth Cone Collapse
J. Neurosci.,
January 1, 2003;
23(1):
175 - 186.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Molnar, G. Lopez-Bendito, J. Small, L. D. Partridge, C. Blakemore, and M. C. Wilson
Normal Development of Embryonic Thalamocortical Connectivity in the Absence of Evoked Synaptic Activity
J. Neurosci.,
December 1, 2002;
22(23):
10313 - 10323.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Bagnard, N. Chounlamountri, A. W. Puschel, and J. Bolz
Axonal Surface Molecules Act in Combination with Semaphorin 3A during the Establishment of Corticothalamic Projections
Cereb Cortex,
March 1, 2001;
11(3):
278 - 285.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Skaliora, R. Adams, and C. Blakemore
Morphology and Growth Patterns of Developing Thalamocortical Axons
J. Neurosci.,
May 15, 2000;
20(10):
3650 - 3662.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. A. Asher, D. A. Morgenstern, P. S. Fidler, K. H. Adcock, A. Oohira, J. E. Braistead, J. M. Levine, R. U. Margolis, J. H. Rogers, and J. W. Fawcett
Neurocan Is Upregulated in Injured Brain and in Cytokine-Treated Astrocytes
J. Neurosci.,
April 1, 2000;
20(7):
2427 - 2438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Mohrmann, M. Werner, H. Hatt, and K. Gottmann
Target-Specific Factors Regulate the Formation of Glutamatergic Transmitter Release Sites in Cultured Neocortical Neurons
J. Neurosci.,
November 15, 1999;
19(22):
10004 - 10013.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R Tuttle, Y Nakagawa, J. Johnson, and D. O'Leary
Defects in thalamocortical axon pathfinding correlate with altered cell domains in Mash-1-deficient mice
Development,
January 5, 1999;
126(9):
1903 - 1916.
[Abstract]
[PDF]
|
|
|
|
|
|
|
F. Mann, V. Zhukareva, A. Pimenta, P. Levitt, and J. Bolz
Membrane-Associated Molecules Guide Limbic and Nonlimbic Thalamocortical Projections
J. Neurosci.,
November 15, 1998;
18(22):
9409 - 9419.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Molnar, R. Adams, A. M. Goffinet, and C. Blakemore
The Role of the First Postmitotic Cortical Cells in the Development of Thalamocortical Innervation in the Reeler Mouse
J. Neurosci.,
August 1, 1998;
18(15):
5746 - 5765.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D Bagnard, M Lohrum, D Uziel, A. Puschel, and J Bolz
Semaphorins act as attractive and repulsive guidance signals during the development of cortical projections
Development,
January 12, 1998;
125(24):
5043 - 5053.
[Abstract]
[PDF]
|
|
|
|
|
|
|
R Tuttle, J. Braisted, L. Richards, and D. O'Leary
Retinal axon guidance by region-specific cues in diencephalon
Development,
January 3, 1998;
125(5):
791 - 801.
[Abstract]
[PDF]
|
|
|
|
|
|
|
V. Castellani and J. Bolz
Membrane-associated molecules regulate the formation of layer-specific cortical circuits
PNAS,
June 24, 1997;
94(13):
7030 - 7035.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D Caric, D Gooday, R. Hill, S. McConnell, and D. Price
Determination of the migratory capacity of embryonic cortical cells lacking the transcription factor Pax-6
Development,
January 12, 1997;
124(24):
5087 - 5096.
[Abstract]
[PDF]
|
|
|
|
|
|
|
J. A. Del Rio, B. Heimrich, H. Super, V. Borrell, M. Frotscher, and E. Soriano
Differential Survival of Cajal-Retzius Cells in Organotypic Cultures of Hippocampus and Neocortex
J. Neurosci.,
November 1, 1996;
16(21):
6896 - 6907.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Henke-Fahle, F. Mann, M. Gotz, K. Wild, and J. Bolz
Dual Action of a Carbohydrate Epitope on Afferent and Efferent Axons in Cortical Development
J. Neurosci.,
July 1, 1996;
16(13):
4195 - 4206.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Price and R. B. Lotto
Influences of the Thalamus on the Survival of Subplate and Cortical Plate Cells in Cultured Embryonic Mouse Brain
J. Neurosci.,
May 15, 1996;
16(10):
3247 - 3255.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
