 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
The Journal of Neuroscience, May 15, 2000, 20(10):3676-3686
Recycling of the Cell Adhesion Molecule L1 in Axonal Growth Cones
Hiroyuki Kamiguchi1, 2 and Vance Lemmon2 1 Developmental Brain Science Group, Brain Science Institute, RIKEN (Institute of Physical and Chemical Research), Wako, Saitama 351-0198, Japan, and 2 Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio 44106-4975
The cell adhesion molecule (CAM) L1 plays crucial roles in axon growth in vitro and in the formation of major axonal tracts in vivo. It is generally thought that CAMs link extracellular immobile ligands with retrogradely moving actin filaments to transmit force that pulls the growth cone forward. However, relatively little is known about the fate of CAMs that have been translocated into the central (C)-domain of the growth cone. We have shown previously that L1 is preferentially endocytosed at the C-domain. In the present study, we further analyze the subcellular distribution of endocytic organelles containing L1 at different time points and demonstrate that internalized L1 is transported into the peripheral (P)-domain of growth cones advancing via an L1-dependent mechanism. Internalized L1 is found in vesicles positioned along microtubules, and the centrifugal transport of these L1-containing vesicles is dependent on dynamic microtubules in the P-domain. Furthermore, we show that endocytosed L1 is reinserted into the plasma membrane at the leading edge of the P-domain. Monitoring recycled L1 reveals that it moves retrogradely on the cell surface into the C-domain. In contrast, the growth cone advancing independently of L1 internalizes and recycles L1 within the C-domain. For the growth cone to advance, the leading edge needs to establish strong adhesive interactions with the substrate while attachments at the rear are released. Recycling L1 from the C-domain to the leading edge provides an effective way to create asymmetric L1-mediated adhesion and therefore would be critical for L1-based growth cone motility.
Key words: neural cell adhesion molecule; L1; axonal growth cone; endocytosis; recycling; microtubule
Copyright © 2000 Society for Neuroscience 0270-6474/00/20103676-11$05.00/0
This article has been cited by other articles:
R. Muramatsu, S. Nakahara, J. Ichikawa, K. Watanabe, N. Matsuki, and R. Koyama
The ratio of 'deleted in colorectal cancer' to 'uncoordinated-5A' netrin-1 receptors on the growth cone regulates mossy fibre directionality
Brain, January 1, 2010; 133(1): 60 - 75.
[Abstract] [Full Text] [PDF]
W. Bu, A. M. Chou, K. B. Lim, T. Sudhaharan, and S. Ahmed
The Toca-1-N-WASP Complex Links Filopodial Formation to Endocytosis
J. Biol. Chem., April 24, 2009; 284(17): 11622 - 11636.
[Abstract] [Full Text] [PDF]
D. Bonanomi, E. F. Fornasiero, G. Valdez, S. Halegoua, F. Benfenati, A. Menegon, and F. Valtorta
Identification of a developmentally regulated pathway of membrane retrieval in neuronal growth cones
J. Cell Sci., November 15, 2008; 121(22): 3757 - 3769.
[Abstract] [Full Text] [PDF]
C. C. Yap, D. Wisco, P. Kujala, Z. M. Lasiecka, J. T. Cannon, M. C. Chang, H. Hirling, J. Klumperman, and B. Winckler
The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM
J. Cell Biol., February 25, 2008; 180(4): 827 - 842.
[Abstract] [Full Text] [PDF]
S. Diestel, D. Schaefer, H. Cremer, and B. Schmitz
NCAM is ubiquitylated, endocytosed and recycled in neurons
J. Cell Sci., November 15, 2007; 120(22): 4035 - 4049.
[Abstract] [Full Text] [PDF]
C. Dequidt, L. Danglot, P. Alberts, T. Galli, D. Choquet, and O. Thoumine
Fast Turnover of L1 Adhesions in Neuronal Growth Cones Involving Both Surface Diffusion and Exo/Endocytosis of L1 Molecules
Mol. Biol. Cell, August 1, 2007; 18(8): 3131 - 3143.
[Abstract] [Full Text] [PDF]
N. E. Winterwood, A. Varzavand, M. N. Meland, L. K. Ashman, and C. S. Stipp
A Critical Role for Tetraspanin CD151 in {alpha}3beta1 and {alpha}6beta4 Integrin-dependent Tumor Cell Functions on Laminin-5
Mol. Biol. Cell, June 1, 2006; 17(6): 2707 - 2721.
[Abstract] [Full Text] [PDF]
J. L. Bartoe, W. L. McKenna, T. K. Quan, B. K. Stafford, J. A. Moore, J. Xia, K. Takamiya, R. L. Huganir, and L. Hinck
Protein interacting with C-kinase 1/protein kinase Calpha-mediated endocytosis converts netrin-1-mediated repulsion to attraction.
J. Neurosci., March 22, 2006; 26(12): 3192 - 3205.
[Abstract] [Full Text] [PDF]
N. Arimura, C. Menager, Y. Kawano, T. Yoshimura, S. Kawabata, A. Hattori, Y. Fukata, M. Amano, Y. Goshima, M. Inagaki, et al.
Phosphorylation by Rho Kinase Regulates CRMP-2 Activity in Growth Cones
Mol. Cell. Biol., November 15, 2005; 25(22): 9973 - 9984.
[Abstract] [Full Text] [PDF]
T. Piazza, E. Cha, I. Bongarzone, S. Canevari, A. Bolognesi, L. Polito, A. Bargellesi, F. Sassi, S. Ferrini, and M. Fabbi
Internalization and recycling of ALCAM/CD166 detected by a fully human single-chain recombinant antibody
J. Cell Sci., April 1, 2005; 118(7): 1515 - 1525.
[Abstract] [Full Text] [PDF]
L. Cheng, K. Itoh, and V. Lemmon
L1-Mediated Branching Is Regulated by Two Ezrin-Radixin-Moesin (ERM)-Binding Sites, the RSLE Region and a Novel Juxtamembrane ERM-Binding Region
J. Neurosci., January 12, 2005; 25(2): 395 - 403.
[Abstract] [Full Text] [PDF]
L. R. Strachan and M. L. Condic
Cranial neural crest recycle surface integrins in a substratum-dependent manner to promote rapid motility
J. Cell Biol., November 8, 2004; 167(3): 545 - 554.
[Abstract] [Full Text] [PDF]
V. J. Tom, M. P. Steinmetz, J. H. Miller, C. M. Doller, and J. Silver
Studies on the Development and Behavior of the Dystrophic Growth Cone, the Hallmark of Regeneration Failure, in an In Vitro Model of the Glial Scar and after Spinal Cord Injury
J. Neurosci., July 21, 2004; 24(29): 6531 - 6539.
[Abstract] [Full Text] [PDF]
J.-F. Bouchard, S. W. Moore, N. X. Tritsch, P. P. Roux, M. Shekarabi, P. A. Barker, and T. E. Kennedy
Protein Kinase A Activation Promotes Plasma Membrane Insertion of DCC from an Intracellular Pool: A Novel Mechanism Regulating Commissural Axon Extension
J. Neurosci., March 24, 2004; 24(12): 3040 - 3050.
[Abstract] [Full Text] [PDF]
T. Tomoda, J. H. Kim, C. Zhan, and M. E. Hatten
Role of Unc51.1 and its binding partners in CNS axon outgrowth
Genes & Dev., March 1, 2004; 18(5): 541 - 558.
[Abstract] [Full Text] [PDF]
A.E. Wiencken-Barger, J. Mavity-Hudson, U. Bartsch, M. Schachner, and V.A. Casagrande
The Role of L1 in Axon Pathfinding and Fasciculation
Cereb Cortex, February 1, 2004; 14(2): 121 - 131.
[Abstract] [Full Text] [PDF]
D. J. Hernandez-Deviez, M. G. Roth, J. E. Casanova, and J. M. Wilson
ARNO and ARF6 Regulate Axonal Elongation and Branching through Downstream Activation of Phosphatidylinositol 4-Phosphate 5-Kinase {alpha}
Mol. Biol. Cell, January 1, 2004; 15(1): 111 - 120.
[Abstract] [Full Text] [PDF]
P. Alberts, R. Rudge, I. Hinners, A. Muzerelle, S. Martinez-Arca, T. Irinopoulou, V. Marthiens, S. Tooze, F. Rathjen, P. Gaspar, et al.
Cross Talk between Tetanus Neurotoxin-insensitive Vesicle-associated Membrane Protein-mediated Transport and L1-mediated Adhesion
Mol. Biol. Cell, October 1, 2003; 14(10): 4207 - 4220.
[Abstract] [Full Text] [PDF]
D. Wisco, E. D. Anderson, M. C. Chang, C. Norden, T. Boiko, H. Folsch, and B. Winckler
Uncovering multiple axonal targeting pathways in hippocampal neurons
J. Cell Biol., September 29, 2003; 162(7): 1317 - 1328.
[Abstract] [Full Text] [PDF]
R. K. Murphey, S. J. Froggett, P. Caruccio, X. Shan-Crofts, T. Kitamoto, and T. A. Godenschwege
Targeted expression of shibirets and semaphorin 1a reveals critical periods for synapse formation in the giant fiber of Drosophila
Development, August 15, 2003; 130(16): 3671 - 3682.
[Abstract] [Full Text] [PDF]
G. R. Phillips, H. Tanaka, M. Frank, A. Elste, L. Fidler, D. L. Benson, and D. R. Colman
{gamma}-Protocadherins Are Targeted to Subsets of Synapses and Intracellular Organelles in Neurons
J. Neurosci., June 15, 2003; 23(12): 5096 - 5104.
[Abstract] [Full Text] [PDF]
D. Kiryushko, T. Kofoed, G. Skladchikova, A. Holm, V. Berezin, and E. Bock
A Synthetic Peptide Ligand of Neural Cell Adhesion Molecule (NCAM), C3d, Promotes Neuritogenesis and Synaptogenesis and Modulates Presynaptic Function in Primary Cultures of Rat Hippocampal Neurons
J. Biol. Chem., March 28, 2003; 278(14): 12325 - 12334.
[Abstract] [Full Text] [PDF]
J. Z. Rappoport and S. M. Simon
Real-time analysis of clathrin-mediated endocytosis during cell migration
J. Cell Sci., March 1, 2003; 116(5): 847 - 855.
[Abstract] [Full Text] [PDF]
P. Steiner, J.-C. F. Sarria, L. Glauser, S. Magnin, S. Catsicas, and H. Hirling
Modulation of receptor cycling by neuron-enriched endosomal protein of 21 kD
J. Cell Biol., June 24, 2002; 157(7): 1197 - 1209.
[Abstract] [Full Text] [PDF]
A. W. Schaefer, Y. Kamei, H. Kamiguchi, E. V. Wong, I. Rapoport, T. Kirchhausen, C. M. Beach, G. Landreth, S. K. Lemmon, and V. Lemmon
L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1
J. Cell Biol., June 24, 2002; 157(7): 1223 - 1232.
[Abstract] [Full Text] [PDF]
H. Kamiguchi and F. Yoshihara
The Role of Endocytic L1 Trafficking in Polarized Adhesion and Migration of Nerve Growth Cones
J. Neurosci., December 1, 2001; 21(23): 9194 - 9203.
[Abstract] [Full Text] [PDF]
C. A. Worby, N. Simonson-Leff, J. C. Clemens, R. P. Kruger, M. Muda, and J. E. Dixon
The Sorting Nexin, DSH3PX1, Connects the Axonal Guidance Receptor, Dscam, to the Actin Cytoskeleton
J. Biol. Chem., November 2, 2001; 276(45): 41782 - 41789.
[Abstract] [Full Text] [PDF]
M. Koroll, F. G. Rathjen, and H. Volkmer
The Neural Cell Recognition Molecule Neurofascin Interacts with Syntenin-1 but Not with Syntenin-2, Both of Which Reveal Self-associating Activity
J. Biol. Chem., March 30, 2001; 276(14): 10646 - 10654.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|