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Volume 17, Number 10,
Issue of May 15, 1997
pp. 3503-3514
Copyright ©1997 Society for Neuroscience
Downregulation of Tetrodotoxin-Resistant Sodium Currents and
Upregulation of a Rapidly Repriming Tetrodotoxin-Sensitive Sodium
Current in Small Spinal Sensory Neurons after Nerve Injury
Received Dec. 11, 1996; revised March 3, 1997; accepted March 5, 1997.
Theodore R. Cummins and
Stephen G. Waxman
Department of Neurology, Yale University School of Medicine, New
Haven, Connecticut 06510, and Neuroscience Research Center, Veterans
Administration Medical Center, West Haven, Connecticut 06516
Clinical and experimental studies have shown that spinal sensory
neurons become hyperexcitable after axonal injury, and
electrophysiological changes have suggested that this may be
attributable to changes in sodium current expression. We have
demonstrated previously that sodium channel -III mRNA levels are
elevated and sodium channel -SNS mRNA levels are reduced in rat
spinal sensory neurons after axotomy. In this study we show that small
(C-type) rat spinal sensory neurons express sodium currents with
dramatically different kinetics after axotomy produced by sciatic nerve
ligation. Uninjured C-type neurons express both slowly inactivating
tetrodotoxin-resistant (TTX-R) sodium current and a fast-inactivating
tetrodotoxin-sensitive (TTX-S) current that reprimes (recovers from
inactivation) slowly. After axotomy, the TTX-R current density was
greatly reduced. No difference was observed in the density of TTX-S
currents after axotomy, and their voltage dependence was not different
from controls. However, TTX-S currents in axotomized neurons reprimed
four times faster than control TTX-S currents. These data indicate that
axotomy of spinal neurons is followed by downregulation of TTX-R
current and by the emergence of a rapidly repriming TTX-S current and suggest that this may be attributable to the upregulation of a sodium
channel isoform that was unexpressed previously in these cells. These
axotomy-induced changes in sodium currents are expected to alter
excitability substantially and could underlie the molecular pathogenesis of some chronic pain syndromes associated with injury to
the axons of spinal sensory neurons.
Key words:
sodium channel;
sodium current;
chronic pain;
axotomy;
dorsal root ganglion;
excitability
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M. Renganathan, T. R. Cummins, W. N. Hormuzdiar, J. A. Black, and S. G. Waxman
Nitric Oxide Is an Autocrine Regulator of Na+ Currents in Axotomized C-Type DRG Neurons
J Neurophysiol,
April 1, 2000;
83(4):
2431 - 2442.
[Abstract]
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M. Michaelis, X. Liu, and W. Janig
Axotomized and Intact Muscle Afferents But No Skin Afferents Develop Ongoing Discharges of Dorsal Root Ganglion Origin after Peripheral Nerve Lesion
J. Neurosci.,
April 1, 2000;
20(7):
2742 - 2748.
[Abstract]
[Full Text]
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I. Kohama, K. Ishikawa, and J. D. Kocsis
Synaptic Reorganization in the Substantia Gelatinosa After Peripheral Nerve Neuroma Formation: Aberrant Innervation of Lamina II Neurons by Abeta Afferents
J. Neurosci.,
February 15, 2000;
20(4):
1538 - 1549.
[Abstract]
[Full Text]
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S. G. Waxman
Multiple Sclerosis as a Neuronal Disease
Arch Neurol,
January 1, 2000;
57(1):
22 - 24.
[Full Text]
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J. A. Black, T. R. Cummins, C. Plumpton, Y. H. Chen, W. Hormuzdiar, J. J. Clare, and S. G. Waxman
Upregulation of a Silent Sodium Channel After Peripheral, but not Central, Nerve Injury in DRG Neurons
J Neurophysiol,
November 1, 1999;
82(5):
2776 - 2785.
[Abstract]
[Full Text]
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R. Amir, M. Michaelis, and M. Devor
Membrane Potential Oscillations in Dorsal Root Ganglion Neurons: Role in Normal Electrogenesis and Neuropathic Pain
J. Neurosci.,
October 1, 1999;
19(19):
8589 - 8596.
[Abstract]
[Full Text]
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V. A. Mitchell, D. M. White, and M. J. Cousins
The Long-Term Effect of Epidural Administration of Butamben Suspension on Nerve Injury-Induced Allodynia in Rats
Anesth. Analg.,
October 1, 1999;
89(4):
989 - 989.
[Abstract]
[Full Text]
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B. Everill and J. D. Kocsis
Reduction in Potassium Currents in Identified Cutaneous Afferent Dorsal Root Ganglion Neurons After Axotomy
J Neurophysiol,
August 1, 1999;
82(2):
700 - 708.
[Abstract]
[Full Text]
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F. Tennigkeit, D. W. F. Schwarz, and E. Puil
Effects of Metabotropic Glutamate Receptor Activation in Auditory Thalamus
J Neurophysiol,
August 1, 1999;
82(2):
718 - 729.
[Abstract]
[Full Text]
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S. G. Waxman, S. Dib-Hajj, T. R. Cummins, and J. A. Black
Sodium channels and pain
PNAS,
July 6, 1999;
96(14):
7635 - 7639.
[Abstract]
[Full Text]
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F. Porreca, J. Lai, D. Bian, S. Wegert, M. H. Ossipov, R. M. Eglen, L. Kassotakis, S. Novakovic, D. K. Rabert, L. Sangameswaran, et al.
A comparison of the potential role of the tetrodotoxin-insensitive sodium channels, PN3/SNS and NaN/SNS2, in rat models of chronic pain
PNAS,
July 6, 1999;
96(14):
7640 - 7644.
[Abstract]
[Full Text]
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P. G. Murphy, L. S. Borthwick, R. S. Johnston, G. Kuchel, and P. M. Richardson
Nature of the Retrograde Signal from Injured Nerves that Induces Interleukin-6 mRNA in Neurons
J. Neurosci.,
May 15, 1999;
19(10):
3791 - 3800.
[Abstract]
[Full Text]
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J. Fjell, T. R. Cummins, K. Fried, J. A. Black, and S. G. Waxman
In Vivo NGF Deprivation Reduces SNS Expression and TTX-R Sodium Currents in IB4-Negative DRG Neurons
J Neurophysiol,
February 1, 1999;
81(2):
803 - 810.
[Abstract]
[Full Text]
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L Djouhri, L Bleazard, and S N Lawson
Association of somatic action potential shape with sensory receptive properties in guinea-pig dorsal root ganglion neurones
J. Physiol.,
December 15, 1998;
513(3):
857 - 872.
[Abstract]
[Full Text]
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T. R. Cummins, J. R. Howe, and S. G. Waxman
Slow Closed-State Inactivation: A Novel Mechanism Underlying Ramp Currents in Cells Expressing the hNE/PN1 Sodium Channel
J. Neurosci.,
December 1, 1998;
18(23):
9607 - 9619.
[Abstract]
[Full Text]
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M. Michaelis, C. Vogel, K.-H. Blenk, A. Arnarson, and W. Janig
Inflammatory Mediators Sensitize Acutely Axotomized Nerve Fibers to Mechanical Stimulation in the Rat
J. Neurosci.,
September 15, 1998;
18(18):
7581 - 7587.
[Abstract]
[Full Text]
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A M Rush, M E Brau, A A Elliott, and J R Elliott
Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia
J. Physiol.,
September 15, 1998;
511(3):
771 - 789.
[Abstract]
[Full Text]
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S. D. Dib-Hajj, L. Tyrrell, J. A. Black, and S. G. Waxman
NaN, a novel voltage-gated Na channel, is expressed preferentially in peripheral sensory neurons and down-regulated after axotomy
PNAS,
July 21, 1998;
95(15):
8963 - 8968.
[Abstract]
[Full Text]
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S. D. Dib-Hajj, J. A. Black, T. R. Cummins, A. M. Kenney, J. D. Kocsis, and S. G. Waxman
Rescue of alpha -SNS Sodium Channel Expression in Small Dorsal Root Ganglion Neurons After Axotomy by Nerve Growth Factor In Vivo
J Neurophysiol,
May 1, 1998;
79(5):
2668 - 2676.
[Abstract]
[Full Text]
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S. N. Macfarlane and H. Sontheimer
Spinal Cord Astrocytes Display a Switch From TTX-Sensitive to TTX-Resistant Sodium Currents After Injury-Induced Gliosis In Vitro
J Neurophysiol,
April 1, 1998;
79(4):
2222 - 2226.
[Abstract]
[Full Text]
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S. D. Novakovic, E. Tzoumaka, J. G. McGivern, M. Haraguchi, L. Sangameswaran, K. R. Gogas, R. M. Eglen, and J. C. Hunter
Distribution of the Tetrodotoxin-Resistant Sodium Channel PN3 in Rat Sensory Neurons in Normal and Neuropathic Conditions
J. Neurosci.,
March 15, 1998;
18(6):
2174 - 2187.
[Abstract]
[Full Text]
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J.-M. Zhang, D. F. Donnelly, X.-J. Song, and R. H. Lamotte
Axotomy Increases the Excitability of Dorsal Root Ganglion Cells With Unmyelinated Axons
J Neurophysiol,
November 1, 1997;
78(5):
2790 - 2794.
[Abstract]
[Full Text]
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T. R. Cummins, S. D. Dib-Hajj, J. A. Black, A. N. Akopian, J. N. Wood, and S. G. Waxman
A Novel Persistent Tetrodotoxin-Resistant Sodium Current In SNS-Null And Wild-Type Small Primary Sensory Neurons
J. Neurosci.,
December 15, 1999;
19(24):
RC43 - RC43.
[Abstract]
[Full Text]
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