 |
 Previous Article | Next Article 
Journal of Neuroscience, Vol 10, 3935-3946, Copyright © 1990 by Society for Neuroscience
Pioneer growth cone steering decisions mediated by single filopodial contacts in situ
TP O'Connor, JS Duerr and D Bentley
Department of Molecular and Cell Biology, University of California, Berkeley 94720.
In grasshopper embryo limb buds, the sibling Ti1 pioneers are the first
neurons to initiate axonogenesis. The pioneer growth cones migrate from the
limb tip to the CNS along a in direction comprising discrete steering
events. Filopodial exploration of the cellular terrain in the vicinity of
the advancing growth cone appears to be important for steering. Some
information is available on the identity of cells and cell types, on
cell-surface characteristics, and on the involvement of basal lamina in
these steering decisions. In the work reported here, we have used
computer-enhanced fluorescence video microscopy to examine filopodial
behavior and the process of growth cone migration and reorientation
resulting from interactions with the normal guidance cues on the in situ
substrate. We observed several different kinds of migration and steering
events, which appear to be related to the absolute and relative affinities
of the contacted substrates. On a relatively homogeneous substrate of
intrasegmental epithelium, growth cones advance by extending veils between
filopodia, as is commonly observed on uniform substrates in vitro. Where
growth cones confront an orthogonal border between substrates of dissimilar
affinity, they remain on the higher-affinity substrate by extending new
branches along it. Subsequently, reorientation in the preferred direction
on the higher-affinity substrate is accomplished by regression of branches
extended in the nonselected direction. By contrast, a single filopodial
contact with a very high-affinity substrate, such as a guidepost neuron,
can reorient a growth cone, even when it is migrating on a favorable
substrate. In this situation, the filopodium that contacts the
high-affinity substrate expands in diameter until it becomes the nascent
axon.
This article has been cited by other articles:
|
|
|
|
 
H. Kohsaka and A. Nose
Target recognition at the tips of postsynaptic filopodia: accumulation and function of Capricious
Development,
April 1, 2009;
136(7):
1127 - 1135.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Dwivedy, F. B. Gertler, J. Miller, C. E. Holt, and C. Lebrand
Ena/VASP function in retinal axons is required for terminal arborization but not pathway navigation
Development,
June 1, 2007;
134(11):
2137 - 2146.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Berghuis, A. M. Rajnicek, Y. M. Morozov, R. A. Ross, J. Mulder, G. M. Urban, K. Monory, G. Marsicano, M. Matteoli, A. Canty, et al.
Hardwiring the Brain: Endocannabinoids Shape Neuronal Connectivity
Science,
May 25, 2007;
316(5828):
1212 - 1216.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. B. Bohil, B. W. Robertson, and R. E. Cheney
Myosin-X is a molecular motor that functions in filopodia formation
PNAS,
August 15, 2006;
103(33):
12411 - 12416.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V Berno, D Porrini, F Castiglioni, M Campiglio, P Casalini, S M Pupa, A Balsari, S Menard, and E Tagliabue
The 67 kDa laminin receptor increases tumor aggressiveness by remodeling laminin-1
Endocr. Relat. Cancer,
June 1, 2005;
12(2):
393 - 406.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Zhang, L.-Q. Jin, J.-Y. Sul, P. G. Haydon, and M. E. Selzer
Live Imaging of Regenerating Lamprey Spinal Axons
Neurorehabil Neural Repair,
March 1, 2005;
19(1):
46 - 57.
[Abstract]
[PDF]
|
|
|
|
|
|
|
S. Gehler, A. E. Shaw, P. D. Sarmiere, J. R. Bamburg, and P. C. Letourneau
Brain-Derived Neurotrophic Factor Regulation of Retinal Growth Cone Filopodial Dynamics Is Mediated through Actin Depolymerizing Factor/Cofilin
J. Neurosci.,
November 24, 2004;
24(47):
10741 - 10749.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Gehler, G. Gallo, E. Veien, and P. C. Letourneau
p75 Neurotrophin Receptor Signaling Regulates Growth Cone Filopodial Dynamics through Modulating RhoA Activity
J. Neurosci.,
May 5, 2004;
24(18):
4363 - 4372.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Brown and P. C. Bridgman
Role of Myosin II in Axon Outgrowth
J. Histochem. Cytochem.,
April 1, 2003;
51(4):
421 - 428.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. T. Legg and T. P. O'Connor
Gradients and Growth Cone Guidance of Grasshopper Neurons
J. Histochem. Cytochem.,
April 1, 2003;
51(4):
445 - 454.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. M. Isbister, P. J. Mackenzie, K. C. W. To, and T. P. O'Connor
Gradient Steepness Influences the Pathfinding Decisions of Neuronal Growth Cones In Vivo
J. Neurosci.,
January 1, 2003;
23(1):
193 - 202.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. J. Dickson
Molecular Mechanisms of Axon Guidance
Science,
December 6, 2002;
298(5600):
1959 - 1964.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. B. Steketee and K. W. Tosney
Three Functionally Distinct Adhesions in Filopodia: Shaft Adhesions Control Lamellar Extension
J. Neurosci.,
September 15, 2002;
22(18):
8071 - 8083.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Bonner and T. P. O'Connor
The Permissive Cue Laminin Is Essential for Growth Cone Turning In Vivo
J. Neurosci.,
December 15, 2001;
21(24):
9782 - 9791.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Steketee, K. Balazovich, and K. W. Tosney
Filopodial Initiation and a Novel Filament-organizing Center, the Focal Ring
Mol. Biol. Cell,
August 1, 2001;
12(8):
2378 - 2395.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. M. Gomez, E. Robles, M.-m. Poo, and N. C. Spitzer
Filopodial Calcium Transients Promote Substrate-Dependent Growth Cone Turning
Science,
March 9, 2001;
291(5510):
1983 - 1987.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
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]
|
|
|
|
|
|
|
M. Polinsky, K. Balazovich, and K. W. Tosney
Identification of an Invariant Response: Stable Contact with Schwann Cells Induces Veil Extension in Sensory Growth Cones
J. Neurosci.,
February 1, 2000;
20(3):
1044 - 1055.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. J. Diefenbach, P. B. Guthrie, H. Stier, B. Billups, and S. B. Kater
Membrane Recycling in the Neuronal Growth Cone Revealed by FM1-43 Labeling
J. Neurosci.,
November 1, 1999;
19(21):
9436 - 9444.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Murray and P. M. Whitington
Effects of roundabout on Growth Cone Dynamics, Filopodial Length, and Growth Cone Morphology at the Midline and throughout the Neuropile
J. Neurosci.,
September 15, 1999;
19(18):
7901 - 7912.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Mallavarapu and T. Mitchison
Regulated Actin Cytoskeleton Assembly at Filopodium Tips Controls Their Extension and Retraction
J. Cell Biol.,
September 6, 1999;
146(5):
1097 - 1106.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P.-m. Lau, R. S. Zucker, and D. Bentley
Induction of Filopodia by Direct Local Elevation of Intracellular Calcium Ion Concentration
J. Cell Biol.,
June 14, 1999;
145(6):
1265 - 1276.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. B. Steketee and K. W. Tosney
Contact with Isolated Sclerotome Cells Steers Sensory Growth Cones by Altering Distinct Elements of Extension
J. Neurosci.,
May 1, 1999;
19(9):
3495 - 3506.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. M. Isbister and T. P. O'Connor
Filopodial Adhesion Does Not Predict Growth Cone Steering Events In Vivo
J. Neurosci.,
April 1, 1999;
19(7):
2589 - 2600.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Isbister, A Tsai, S. Wong, A. Kolodkin, and T. O'Connor
Discrete roles for secreted and transmembrane semaphorins in neuronal growth cone guidance in vivo
Development,
January 5, 1999;
126(9):
2007 - 2019.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. Amieva, P Litman, L Huang, E Ichimaru, and H Furthmayr
Disruption of dynamic cell surface architecture of NIH3T3 fibroblasts by the N-terminal domains of moesin and ezrin: in vivo imaging with GFP fusion proteins
J. Cell Sci.,
January 1, 1999;
112(1):
111 - 125.
[Abstract]
[PDF]
|
|
|
|
|
|
|
Q. Wang and J. Q. Zheng
cAMP-Mediated Regulation of Neurotrophin-Induced Collapse of Nerve Growth Cones
J. Neurosci.,
July 1, 1998;
18(13):
4973 - 4984.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. H. J. Aarts, L. H. Schrama, W. J. Hage, J. L. Bos, W. H. Gispen, and P. Schotman
B-50/GAP-43-induced Formation of Filopodia Depends on Rho-GTPase
Mol. Biol. Cell,
June 1, 1998;
9(6):
1279 - 1292.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
Y.-m. E. Wang, P. Esbensen, and D. Bentley
Arginine Kinase Expression and Localization in Growth Cone Migration
J. Neurosci.,
February 1, 1998;
18(3):
987 - 998.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P Lamoureux, R. Buxbaum, and S. Heidemann
Axonal outgrowth of cultured neurons is not limited by growth cone competition
J. Cell Sci.,
January 11, 1998;
111(21):
3245 - 3252.
[Abstract]
[PDF]
|
|
|
|
|
|
|
T. B. Kuhn, C. V. Williams, P. Dou, and S. B. Kater
Laminin Directs Growth Cone Navigation via Two Temporally and Functionally Distinct Calcium Signals
J. Neurosci.,
January 1, 1998;
18(1):
184 - 194.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Rabinovitz and A. M. Mercurio
The Integrin {alpha}6{beta}4 Functions in Carcinoma Cell Migration on Laminin-1 by Mediating the Formation and Stabilization of Actin-containing Motility Structures
J. Cell Biol.,
December 29, 1997;
139(7):
1873 - 1884.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. W. Grabham and D. J. Goldberg
Nerve Growth Factor Stimulates the Accumulation of beta 1 Integrin at the Tips of Filopodia in the Growth Cones of Sympathetic Neurons
J. Neurosci.,
July 15, 1997;
17(14):
5455 - 5465.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Wang and E. R. Macagno
The Establishment of Peripheral Sensory Arbors in the Leech: In Vivo Time-Lapse Studies Reveal a Highly Dynamic Process
J. Neurosci.,
April 1, 1997;
17(7):
2408 - 2419.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Wong, W. Yu, and T. O'Connor
Transmembrane grasshopper Semaphorin I promotes axon outgrowth in vivo
Development,
January 9, 1997;
124(18):
3597 - 3607.
[Abstract]
[PDF]
|
|
|
|
|
|
|
L Erskine and C. McCaig
Integrated interactions between chondroitin sulphate proteoglycans and weak dc electric fields regulate nerve growth cone guidance in vitro
J. Cell Sci.,
January 8, 1997;
110(16):
1957 - 1965.
[Abstract]
[PDF]
|
|
|
|
|
|
|
M. E. Dailey and S. J Smith
The Dynamics of Dendritic Structure in Developing Hippocampal Slices
J. Neurosci.,
May 1, 1996;
16(9):
2983 - 2994.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. Chang, K. Zachow, and D Bentley
Expression of epithelial alkaline phosphatase in segmentally iterated bands during grasshopper limb morphogenesis
Development,
January 6, 1993;
118(2):
651 - 663.
[Abstract]
[PDF]
|
|
|
|
|
