 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
Volume 17, Number 18, Issue of September 15, 1997 pp. 7025-7036
Copyright ©1997 Society for NeuroscienceMorphogenesis of the Node of Ranvier: Co-Clusters of Ankyrin and Ankyrin-Binding Integral Proteins Define Early Developmental Intermediates
Received March 20, 1997; revised May 29, 1997; accepted July 9, 1997.
Stephen Lambert, Jonathan Q. Davis , and Vann Bennett Department of Cell Biology and the Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina 27710
AnkyrinG 480/270 kDa and three ankyrin-binding integral membrane proteins (neurofascin, NrCAM, and the voltage-dependent sodium channel) colocalize within a specialized domain of the spectrin-actin network found at axonal segments of nodes of Ranvier in myelinated axons. Before myelination in embryonic nerves, ankyrinG 480/270 kDa and the related ankyrin isoform ankyrinB 440 kDa are co-expressed along with NrCAM in an abundant, continuous distribution along the length of axons. This study has resolved intermediate stages in the developmental transition from a continuous distribution of ankyrinG 480/270 kDa in all axons to a highly polarized localization at the node of Ranvier in the developing rat sciatic nerve. The first detected event is formation of clusters containing the cell adhesion molecules neurofascin and NrCAM at sites independent of myelin-associated glycoprotein (MAG)-staining Schwann cell processes. Subsequent steps involve recruitment of ankyrinG 480/270 kDa and the voltage-dependent sodium channel to cluster sites containing cell adhesion molecules, and elaboration of MAG-staining Schwann cell processes adjacent to these cluster sites. Formation of the mature node of Ranvier results from the fusion of asynchronously formed pairs of clusters associated with MAG-positive Schwann cells flanking the site of presumed node formation. Studies with the hypomyelinating mutant mouse trembler demonstrate that the elaboration of compact myelin is not required for the formation of these clustered nodal intermediates. Clustering of neurofascin and NrCAM precedes redistribution of ankyrinG 480/270 kDa and the voltage-dependent sodium channel, suggesting that the adhesion molecules define the initial site for subsequent assembly of ankyrin and the voltage-dependent sodium channel.
Key words: node of Ranvier; cell adhesion molecules; ankyrin; voltage-dependent sodium channel; myelination; trembler mutant
This article has been cited by other articles:
B. Zonta, S. Tait, S. Melrose, H. Anderson, S. Harroch, J. Higginson, D. L. Sherman, and P. J. Brophy
Glial and neuronal isoforms of Neurofascin have distinct roles in the assembly of nodes of Ranvier in the central nervous system
J. Cell Biol., October 22, 2008; 181(7): 1169 - 1177.
[Abstract] [Full Text] [PDF]
J. J. P. Alix, A. C. Dolphin, and R. Fern
Vesicular apparatus, including functional calcium channels, are present in developing rodent optic nerve axons and are required for normal node of Ranvier formation
J. Physiol., September 1, 2008; 586(17): 4069 - 4089.
[Abstract] [Full Text] [PDF]
K. Susuki and M. N. Rasband
Spectrin and Ankyrin-Based Cytoskeletons at Polarized Domains in Myelinated Axons
Experimental Biology and Medicine, April 1, 2008; 233(4): 394 - 400.
[Abstract] [Full Text] [PDF]
Y. Dzhashiashvili, Y. Zhang, J. Galinska, I. Lam, M. Grumet, and J. L. Salzer
Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms
J. Cell Biol., June 21, 2007; 177(5): 857 - 870.
[Abstract] [Full Text] [PDF]
Y. Eshed, K. Feinberg, D. J. Carey, and E. Peles
Secreted gliomedin is a perinodal matrix component of peripheral nerves
J. Cell Biol., May 7, 2007; 177(3): 551 - 562.
[Abstract] [Full Text] [PDF]
B. Maertens, D. Hopkins, C.-W. Franzke, D. R. Keene, L. Bruckner-Tuderman, D. S. Greenspan, and M. Koch
Cleavage and Oligomerization of Gliomedin, a Transmembrane Collagen Required for Node of Ranvier Formation
J. Biol. Chem., April 6, 2007; 282(14): 10647 - 10659.
[Abstract] [Full Text] [PDF]
Y. Yang, Y. Ogawa, K. L. Hedstrom, and M. N. Rasband
{beta}IV spectrin is recruited to axon initial segments and nodes of Ranvier by ankyrinG
J. Cell Biol., February 12, 2007; 176(4): 509 - 519.
[Abstract] [Full Text] [PDF]
D. S. Garbe, A. Das, R. R. Dubreuil, and G. J. Bashaw
{beta}-Spectrin functions independently of Ankyrin to regulate the establishment and maintenance of axon connections in the Drosophila embryonic CNS
Development, January 15, 2007; 134(2): 273 - 284.
[Abstract] [Full Text] [PDF]
O. W. Howell, A. Palser, A. Polito, S. Melrose, B. Zonta, C. Scheiermann, A. J. Vora, P. J. Brophy, and R. Reynolds
Disruption of neurofascin localization reveals early changes preceding demyelination and remyelination in multiple sclerosis
Brain, December 1, 2006; 129(12): 3173 - 3185.
[Abstract] [Full Text] [PDF]
M. C. Inda, J. DeFelipe, and A. Munoz
Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells
PNAS, February 21, 2006; 103(8): 2920 - 2925.
[Abstract] [Full Text] [PDF]
J. K. Huang, G. R. Phillips, A. D. Roth, L. Pedraza, W. Shan, W. Belkaid, S. Mi, A. Fex-Svenningsen, L. Florens, J. R. Yates III, et al.
Glial Membranes at the Node of Ranvier Prevent Neurite Outgrowth
Science, December 16, 2005; 310(5755): 1813 - 1817.
[Abstract] [Full Text] [PDF]
S. Occhi, D. Zambroni, U. Del Carro, S. Amadio, E. E. Sirkowski, S. S. Scherer, K. P. Campbell, S. A. Moore, Z.-L. Chen, S. Strickland, et al.
Both Laminin and Schwann Cell Dystroglycan Are Necessary for Proper Clustering of Sodium Channels at Nodes of Ranvier
J. Neurosci., October 12, 2005; 25(41): 9418 - 9427.
[Abstract] [Full Text] [PDF]
J. J. Devaux and S. S. Scherer
Altered Ion Channels in an Animal Model of Charcot-Marie-Tooth Disease Type IA
J. Neurosci., February 9, 2005; 25(6): 1470 - 1480.
[Abstract] [Full Text] [PDF]
D. P. McEwen and L. L. Isom
Heterophilic Interactions of Sodium Channel {beta}1 Subunits with Axonal and Glial Cell Adhesion Molecules
J. Biol. Chem., December 10, 2004; 279(50): 52744 - 52752.
[Abstract] [Full Text] [PDF]
G. Corfas, M. O. Velardez, C.-P. Ko, N. Ratner, and E. Peles
Mechanisms and Roles of Axon-Schwann Cell Interactions
J. Neurosci., October 20, 2004; 24(42): 9250 - 9260.
[Full Text] [PDF]
Y. Yang, S. Lacas-Gervais, D. K. Morest, M. Solimena, and M. N. Rasband
{beta}IV Spectrins Are Essential for Membrane Stability and the Molecular Organization of Nodes of Ranvier
J. Neurosci., August 18, 2004; 24(33): 7230 - 7240.
[Abstract] [Full Text] [PDF]
C. Bonnon, L. Goutebroze, N. Denisenko-Nehrbass, J.-A. Girault, and C. Faivre-Sarrailh
The Paranodal Complex of F3/Contactin and Caspr/Paranodin Traffics to the Cell Surface via a Non-conventional Pathway
J. Biol. Chem., November 28, 2003; 278(48): 48339 - 48347.
[Abstract] [Full Text] [PDF]
A. W. Custer, K. Kazarinova-Noyes, T. Sakurai, X. Xu, W. Simon, M. Grumet, and P. Shrager
The Role of the Ankyrin-Binding Protein NrCAM in Node of Ranvier Formation
J. Neurosci., November 5, 2003; 23(31): 10032 - 10039.
[Abstract] [Full Text] [PDF]
C. L. Gatto, B. J. Walker, and S. Lambert
Local ERM activation and dynamic growth cones at Schwann cell tips implicated in efficient formation of nodes of Ranvier
J. Cell Biol., August 4, 2003; 162(3): 489 - 498.
[Abstract] [Full Text] [PDF]
G. Lemaillet, B. Walker, and S. Lambert
Identification of a Conserved Ankyrin-binding Motif in the Family of Sodium Channel {alpha} Subunits
J. Biol. Chem., July 18, 2003; 278(30): 27333 - 27339.
[Abstract] [Full Text] [PDF]
S. J. Bailey, M. A. Stocksley, A. Buckel, C. Young, and C. R. Slater
Voltage-Gated Sodium Channels and AnkyrinG Occupy a Different Postsynaptic Domain from Acetylcholine Receptors from an Early Stage of Neuromuscular Junction Maturation in Rats
J. Neurosci., March 15, 2003; 23(6): 2102 - 2111.
[Abstract] [Full Text] [PDF]
T. Boiko, A. Van Wart, J. H. Caldwell, S. R. Levinson, J. S. Trimmer, and G. Matthews
Functional Specialization of the Axon Initial Segment by Isoform-Specific Sodium Channel Targeting
J. Neurosci., March 15, 2003; 23(6): 2306 - 2313.
[Abstract] [Full Text] [PDF]
S. M. Curristin, A. Cao, W. B. Stewart, H. Zhang, J. A. Madri, J. S. Morrow, and L. R. Ment
Disrupted synaptic development in the hypoxic newborn brain
PNAS, November 26, 2002; 99(24): 15729 - 15734.
[Abstract] [Full Text] [PDF]
M. N. Rasband, E. W. Park, D. Zhen, M. I. Arbuckle, S. Poliak, E. Peles, S. G.N. Grant, and J. S. Trimmer
Clustering of neuronal potassium channels is independent of their interaction with PSD-95
J. Cell Biol., November 25, 2002; 159(4): 663 - 672.
[Abstract] [Full Text] [PDF]
M. Bouzidi, N. Tricaud, P. Giraud, E. Kordeli, G. Caillol, C. Deleuze, F. Couraud, and G. Alcaraz
Interaction of the Nav1.2a Subunit of the Voltage-dependent Sodium Channel with Nodal AnkyrinG. IN VITRO MAPPING OF THE INTERACTING DOMAINS AND ASSOCIATION IN SYNAPTOSOMES
J. Biol. Chem., August 2, 2002; 277(32): 28996 - 29004.
[Abstract] [Full Text] [PDF]
L. Gollan, H. Sabanay, S. Poliak, E. O. Berglund, B. Ranscht, and E. Peles
Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr
J. Cell Biol., June 24, 2002; 157(7): 1247 - 1256.
[Abstract] [Full Text] [PDF]
C. Gagelin, B. Constantin, C. Deprette, M.-A. Ludosky, M. Recouvreur, J. Cartaud, C. Cognard, G. Raymond, and E. Kordeli
Identification of AnkG107, a Muscle-specific Ankyrin-G Isoform
J. Biol. Chem., April 5, 2002; 277(15): 12978 - 12987.
[Abstract] [Full Text] [PDF]
E. J. Arroyo, T. Xu, J. Grinspan, S. Lambert, S. R. Levinson, P. J. Brophy, E. Peles, and S. S. Scherer
Genetic Dysmyelination Alters the Molecular Architecture of the Nodal Region
J. Neurosci., March 1, 2002; 22(5): 1726 - 1737.
[Abstract] [Full Text] [PDF]
C. Mathis, N. Denisenko-Nehrbass, J.-A. Girault, and E. Borrelli
Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions
Development, December 1, 2001; 128(23): 4881 - 4890.
[Abstract] [Full Text] [PDF]
C. F. Ratcliffe, R. E. Westenbroek, R. Curtis, and W. A. Catterall
Sodium channel {beta}1 and {beta}3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain
J. Cell Biol., July 23, 2001; 154(2): 427 - 434.
[Abstract] [Full Text] [PDF]
M. I. More, F.-P. Kirsch, and F. G. Rathjen
Targeted ablation of NrCAM or ankyrin-B results in disorganized lens fibers leading to cataract formation
J. Cell Biol., July 9, 2001; 154(1): 187 - 196.
[Abstract] [Full Text] [PDF]
V. Bennett and A. J. Baines
Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues
Physiol Rev, July 1, 2001; 81(3): 1353 - 1392.
[Abstract] [Full Text] [PDF]
C. V. Melendez-Vasquez, J. C. Rios, G. Zanazzi, S. Lambert, A. Bretscher, and J. L. Salzer
Nodes of Ranvier form in association with ezrin-radixin-moesin (ERM)-positive Schwann cell processes
PNAS, January 30, 2001; 98(3): 1235 - 1240.
[Abstract] [Full Text] [PDF]
S. M. Jenkins, K. Kizhatil, N. R. Kramarcy, A. Sen, R. Sealock, and V. Bennett
FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons
J. Cell Sci., January 11, 2001; 114(21): 3823 - 3835.
[Abstract] [Full Text] [PDF]
S. Berghs, D. Aggujaro, R. Dirkx , Jr., E. Maksimova, P. Stabach, J.-M. Hermel, J.-P. Zhang, W. Philbrick, V. Slepnev, T. Ort, et al.
{beta}IV Spectrin, a New Spectrin Localized at Axon Initial Segments and Nodes of Ranvier in the Central and Peripheral Nervous System
J. Cell Biol., November 20, 2000; 151(5): 985 - 1002.
[Abstract] [Full Text] [PDF]
S. Tait, F. Gunn-Moore, J. M. Collinson, J. Huang, C. Lubetzki, L. Pedraza, D. L. Sherman, D. R. Colman, and P. J. Brophy
An Oligodendrocyte Cell Adhesion Molecule at the Site of Assembly of the Paranodal Axo-Glial Junction
J. Cell Biol., August 7, 2000; 150(3): 657 - 666.
[Abstract] [Full Text] [PDF]
B. D. Trapp and G. J. Kidd
Axo-Glial Septate Junctions: The Maestro of Nodal Formation and Myelination?
J. Cell Biol., August 7, 2000; 150(3): F97 - F100.
[Abstract] [Full Text] [PDF]
M. Bouley, M.-Z. Tian, K. Paisley, Y.-C. Shen, J. D. Malhotra, and M. Hortsch
The L1-Type Cell Adhesion Molecule Neuroglian Influences the Stability of Neural Ankyrin in the Drosophila Embryo But Not Its Axonal Localization
J. Neurosci., June 15, 2000; 20(12): 4515 - 4523.
[Abstract] [Full Text] [PDF]
C. Faivre-Sarrailh, F. Gauthier, N. Denisenko-Nehrbass, A. Le Bivic, G. Rougon, and J.-A. Girault
The Glycosylphosphatidyl Inositol-anchored Adhesion Molecule F3/Contactin Is Required for Surface Transport of Paranodin/Contactin-associated Protein (caspr)
J. Cell Biol., April 17, 2000; 149(2): 491 - 502.
[Abstract] [Full Text] [PDF]
M. De Matteis and J. Morrow
Spectrin tethers and mesh in the biosynthetic pathway
J. Cell Sci., January 7, 2000; 113(13): 2331 - 2343.
[Abstract] [PDF]
J. L. Dupree, J.-A. Girault, and B. Popko
Axo-glial Interactions Regulate the Localization of Axonal Paranodal Proteins
J. Cell Biol., December 13, 1999; 147(6): 1145 - 1152.
[Abstract] [Full Text] [PDF]
D. Zhou, S. Lambert, P. L. Malen, S. Carpenter, L. M. Boland, and V. Bennett
AnkyrinG Is Required for Clustering of Voltage-gated Na Channels at Axon Initial Segments and for Normal Action Potential Firing
J. Cell Biol., November 30, 1998; 143(5): 1295 - 1304.
[Abstract] [Full Text] [PDF]
P. Scotland, D. Zhou, H. Benveniste, and V. Bennett
Nervous System Defects of AnkyrinB (-/-) Mice Suggest Functional Overlap between the Cell Adhesion Molecule L1 and 440-kD AnkyrinB in Premyelinated Axons
J. Cell Biol., November 30, 1998; 143(5): 1305 - 1315.
[Abstract] [Full Text] [PDF]
X. Zhang and V. Bennett
Restriction of 480/270-kD Ankyrin G to Axon Proximal Segments Requires Multiple Ankyrin G-specific Domains
J. Cell Biol., September 21, 1998; 142(6): 1571 - 1581.
[Abstract] [Full Text] [PDF]
A. G. Koszowski, G. C. Owens, and S. R. Levinson
The Effect of the Mouse Mutation Claw Paw on Myelination and Nodal Frequency in Sciatic Nerves
J. Neurosci., August 1, 1998; 18(15): 5859 - 5868.
[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]
S. M. Jenkins and V. Bennett
Developing nodes of Ranvier are defined by ankyrin-G clustering and are independent of paranodal axoglial adhesion
PNAS, February 19, 2002; 99(4): 2303 - 2308.
[Abstract] [Full Text] [PDF]
S. M. Jenkins and V. Bennett
Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments
J. Cell Biol., November 26, 2001; 155(5): 739 - 746.
[Abstract] [Full Text] [PDF]
M. Komada and P. Soriano
{beta}IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier
J. Cell Biol., January 21, 2002; 156(2): 337 - 348.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|