 |
Previous Article | Next Article 
The Journal of Neuroscience, January 1, 1998, 18(1):36-47
Potassium Channel Distribution, Clustering, and Function in
Remyelinating Rat Axons
Matthew N.
Rasband1,
James S.
Trimmer3,
Thomas
L.
Schwarz4,
S. Rock
Levinson5,
Mark H.
Ellisman6,
Melitta
Schachner7, and
Peter
Shrager2
Departments of 1 Biochemistry and Biophysics and
2 Neurobiology and Anatomy, University of Rochester Medical
Center, Rochester, New York 14642, 3 Department of
Biochemistry and Cell Biology, State University of New York, Stony
Brook, New York 11794, 4 Department of Molecular and
Cellular Physiology, Beckman Center, Stanford University, Stanford,
California 94305, 5 Health Sciences Center, University of
Colorado, Denver, Colorado 80262, 6 Department of
Neurosciences, University of California San Diego, La Jolla, California
92093-0608, and 7 Zentrum fur Moleculare Neurobiologie,
Universitat Hamburg, Hamburg, Germany D-20246
The K+ channel -subunits Kv1.1 and Kv1.2 and
the cytoplasmic -subunit Kv 2 were detected by immunofluorescence
microscopy and found to be colocalized at juxtaparanodes in normal
adult rat sciatic nerve. After demyelination by intraneural injection of lysolecithin, and during remyelination, the subcellular
distributions of Kv1.1, Kv1.2, and Kv 2 were reorganized. At 6 d
postinjection (dpi), axons were stripped of myelin, and
K+ channels were found to be dispersed across zones
that extended into both nodal and internodal regions; a few days later
they were undetectable. By 10 dpi, remyelination was underway, but Kv1.1 immunoreactivity was absent at newly forming nodes of Ranvier. By
14 dpi, K+ channels were detected but were in the
nodal gap between Schwann cells. By 19 dpi, most new nodes had Kv1.1,
Kv1.2, and Kv 2, which precisely colocalized. However, this nodal
distribution was transient. By 24 dpi, the majority of
K+ channels was clustered within paranodal regions
of remyelinated axons, leaving a gap that overlapped with
Na+ channel immunoreactivity. Inhibition of Schwann
cell proliferation delayed both remyelination and the development of
the K+ channel distributions described. Conduction
studies indicate that neither 4-aminopyridine (4-AP) nor
tetraethylammonium alters normal nerve conduction. However, during
remyelination, 4-AP profoundly increased both compound action potential
amplitude and duration. The level of this effect matched closely the
nodal presence of these voltage-dependent K+
channels. Our results suggest that K+ channels may
have a significant effect on conduction during remyelination and that
Schwann cells are important in K+ channel
redistribution and clustering.
Key words:
potassium channels; demyelination; remyelination; Schwann
cells; axons; node of Ranvier
Copyright © 1998 Society for Neuroscience 0270-6474/98/18136-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
M. N. Miller, B. W. Okaty, and S. B. Nelson
Region-Specific Spike-Frequency Acceleration in Layer 5 Pyramidal Neurons Mediated by Kv1 Subunits
J. Neurosci.,
December 17, 2008;
28(51):
13716 - 13726.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Vacher, D. P. Mohapatra, and J. S. Trimmer
Localization and Targeting of Voltage-Dependent Ion Channels in Mammalian Central Neurons
Physiol Rev,
October 1, 2008;
88(4):
1407 - 1447.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Biernaskie, J. S. Sparling, J. Liu, C. P. Shannon, J. R. Plemel, Y. Xie, F. D. Miller, and W. Tetzlaff
Skin-Derived Precursors Generate Myelinating Schwann Cells That Promote Remyelination and Functional Recovery after Contusion Spinal Cord Injury
J. Neurosci.,
September 5, 2007;
27(36):
9545 - 9559.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Eftekharpour, S. Karimi-Abdolrezaee, J. Wang, H. El Beheiry, C. Morshead, and M. G. Fehlings
Myelination of Congenitally Dysmyelinated Spinal Cord Axons by Adult Neural Precursor Cells Results in Formation of Nodes of Ranvier and Improved Axonal Conduction
J. Neurosci.,
March 28, 2007;
27(13):
3416 - 3428.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Bai, E. Ianokova, Q. Pu, K. Ghandour, R. Levinson, J.-J. Martin, C. Ceuterick-de Groote, R. Mazanec, P. Seeman, M. E. Shy, et al.
Effect of an R69C Mutation in the Myelin Protein Zero Gene on Myelination and Ion Channel Subtypes
Arch Neurol,
December 1, 2006;
63(12):
1787 - 1794.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Coman, M. S. Aigrot, D. Seilhean, R. Reynolds, J. A. Girault, B. Zalc, and C. Lubetzki
Nodal, paranodal and juxtaparanodal axonal proteins during demyelination and remyelination in multiple sclerosis
Brain,
December 1, 2006;
129(12):
3186 - 3195.
[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]
|
 |
|

|
 |

|
 |
 
K. A. Kleopa, L. B. Elman, B. Lang, A. Vincent, and S. S. Scherer
Neuromyotonia and limbic encephalitis sera target mature Shaker-type K+ channels: subunit specificity correlates with clinical manifestations
Brain,
June 1, 2006;
129(6):
1570 - 1584.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Schwarz, G. Glassmeier, E. C. Cooper, T.-C Kao, H. Nodera, D. Tabuena, R. Kaji, and H. Bostock
KCNQ channels mediate IKs, a slow K+ current regulating excitability in the rat node of Ranvier
J. Physiol.,
May 15, 2006;
573(1):
17 - 34.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Pan, T. Kao, Z. Horvath, J. Lemos, J.-Y. Sul, S. D. Cranstoun, V. Bennett, S. S. Scherer, and E. C. Cooper
A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon.
J. Neurosci.,
March 8, 2006;
26(10):
2599 - 2613.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Sinha, S. Karimi-Abdolrezaee, A. A. Velumian, and M. G. Fehlings
Functional Changes in Genetically Dysmyelinated Spinal Cord Axons of Shiverer Mice: Role of Juxtaparanodal Kv1 Family K+ Channels
J Neurophysiol,
March 1, 2006;
95(3):
1683 - 1695.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Sasaki, J. A. Black, K. L. Lankford, H. A. Tokuno, S. G. Waxman, and J. D. Kocsis
Molecular Reconstruction of Nodes of Ranvier after Remyelination by Transplanted Olfactory Ensheathing Cells in the Demyelinated Spinal Cord
J. Neurosci.,
February 8, 2006;
26(6):
1803 - 1812.
[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]
|
 |
|

|
 |

|
 |
 
T. Marqueste, J.-R. Alliez, O. Alluin, Y. Jammes, and P. Decherchi
Neuromuscular rehabilitation by treadmill running or electrical stimulation after peripheral nerve injury and repair
J Appl Physiol,
May 1, 2004;
96(5):
1988 - 1995.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Shen, S. Hernandez-Lopez, T. Tkatch, J. E. Held, and D. J. Surmeier
Kv1.2-Containing K+ Channels Regulate Subthreshold Excitability of Striatal Medium Spiny Neurons
J Neurophysiol,
March 1, 2004;
91(3):
1337 - 1349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ishibashi, L. Ding, K. Ikenaka, Y. Inoue, K. Miyado, E. Mekada, and H. Baba
Tetraspanin Protein CD9 Is a Novel Paranodal Component Regulating Paranodal Junctional Formation
J. Neurosci.,
January 7, 2004;
24(1):
96 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. E. Hanak, E. M. Reilly, J. Wotanis, B. Zhu, C. Pulicicchio, K. McMonagle-Strucko, J. G. Wettstein, and M. D. Black
An Electrophysiological Model of Spinal Transmission Deficits in Mouse Experimental Autoimmune Encephalomyelitis
J. Pharmacol. Exp. Ther.,
January 1, 2004;
308(1):
214 - 220.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Poliak, D. Salomon, H. Elhanany, H. Sabanay, B. Kiernan, L. Pevny, C. L. Stewart, X. Xu, S.-Y. Chiu, P. Shrager, et al.
Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1
J. Cell Biol.,
September 15, 2003;
162(6):
1149 - 1160.
[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]
|
 |
|

|
 |

|
 |
 
Y. Xu, N. Chiamvimonvat, A. E. Vazquez, S. Akunuru, N. Ratner, and E. N. Yamoah
Gene-Targeted Deletion of Neurofibromin Enhances the Expression of a Transient Outward K+ Current in Schwann Cells: A Protein Kinase A-Mediated Mechanism
J. Neurosci.,
November 1, 2002;
22(21):
9194 - 9202.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Akhtar, O. Shamotienko, M. Papakosta, F. Ali, and J. O. Dolly
Characteristics of Brain Kv1 Channels Tailored to Mimic Native Counterparts by Tandem Linkage of alpha Subunits. IMPLICATIONS FOR K+ CHANNELOPATHIES
J. Biol. Chem.,
May 3, 2002;
277(19):
16376 - 16382.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Devaux, M. Gola, G. Jacquet, and M. Crest
Effects of K+ Channel Blockers on Developing Rat Myelinated CNS Axons: Identification of Four Types of K+ Channels
J Neurophysiol,
March 1, 2002;
87(3):
1376 - 1385.
[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]
|
 |
|

|
 |

|
 |
 
M. N. Rasband, E. W. Park, T. W. Vanderah, J. Lai, F. Porreca, and J. S. Trimmer
Distinct potassium channels on pain-sensing neurons
PNAS,
November 6, 2001;
98(23):
13373 - 13378.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Martin, A. K. Levine, Z. J. Chen, Y. Ughrin, and J. M. Levine
Deposition of the NG2 Proteoglycan at Nodes of Ranvier in the Peripheral Nervous System
J. Neurosci.,
October 15, 2001;
21(20):
8119 - 8128.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Beeton, J. Barbaria, P. Giraud, J. Devaux, A.-M. Benoliel, M. Gola, J. M. Sabatier, D. Bernard, M. Crest, and E. Beraud
Selective Blocking of Voltage-Gated K+ Channels Improves Experimental Autoimmune Encephalomyelitis and Inhibits T Cell Activation
J. Immunol.,
January 15, 2001;
166(2):
936 - 944.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Tkatch, G. Baranauskas, and D. J. Surmeier
Kv4.2 mRNA Abundance and A-Type K+ Current Amplitude Are Linearly Related in Basal Ganglia and Basal Forebrain Neurons
J. Neurosci.,
January 15, 2000;
20(2):
579 - 588.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. G. M. Jugloff, R. Khanna, L. C. Schlichter, and O. T. Jones
Internalization of the Kv1.4 Potassium Channel Is Suppressed by Clustering Interactions with PSD-95
J. Biol. Chem.,
January 14, 2000;
275(2):
1357 - 1364.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Tiffany, L. N. Manganas, E. Kim, Y.-P. Hsueh, M. Sheng, and J. S. Trimmer
PSD-95 and SAP97 Exhibit Distinct Mechanisms for Regulating K+ Channel Surface Expression and Clustering
J. Cell Biol.,
January 10, 2000;
148(1):
147 - 158.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. N. Rasband, E. Peles, J. S. Trimmer, S. R. Levinson, S. E. Lux, and P. Shrager
Dependence of Nodal Sodium Channel Clustering on Paranodal Axoglial Contact in the Developing CNS
J. Neurosci.,
September 1, 1999;
19(17):
7516 - 7528.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Weber, U. Bartsch, M. N. Rasband, R. Czaniera, Y. Lang, H. Bluethmann, R. U. Margolis, S. R. Levinson, P. Shrager, D. Montag, et al.
Mice Deficient for Tenascin-R Display Alterations of the Extracellular Matrix and Decreased Axonal Conduction Velocities in the CNS
J. Neurosci.,
June 1, 1999;
19(11):
4245 - 4262.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Vabnick, J. S. Trimmer, T. L. Schwarz, S. R. Levinson, D. Risal, and P. Shrager
Dynamic Potassium Channel Distributions during Axonal Development Prevent Aberrant Firing Patterns
J. Neurosci.,
January 15, 1999;
19(2):
747 - 758.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Sobko, A. Peretz, O. Shirihai, S. Etkin, V. Cherepanova, D. Dagan, and B. Attali
Heteromultimeric Delayed-Rectifier K+ Channels in Schwann Cells: Developmental Expression and Role in Cell Proliferation
J. Neurosci.,
December 15, 1998;
18(24):
10398 - 10408.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Zhou, C.-L. Zhang, A. Messing, and S. Y. Chiu
Temperature-Sensitive Neuromuscular Transmission in Kv1.1 Null Mice: Role of Potassium Channels under the Myelin Sheath in Young Nerves
J. Neurosci.,
September 15, 1998;
18(18):
7200 - 7215.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. N. Manganas, S. Akhtar, D. E. Antonucci, C. R. Campomanes, J. O. Dolly, and J. S. Trimmer
Episodic Ataxia Type-1 Mutations in the Kv1.1 Potassium Channel Display Distinct Folding and Intracellular Trafficking Properties
J. Biol. Chem.,
December 21, 2001;
276(52):
49427 - 49434.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|