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PMID: 15760941 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Electrophysiological properties of two axonal sodium channels, Nav1.2 and Nav1.6, expressed in mouse spinal sensory neurones.

The Journal of physiology ·Vol. 564 ·No. Pt 3 ·2005-05-01 ·Pages 803-15

Rush AM, Dib-Hajj SD, Waxman SG

Abstract

Sodium channels Na(v)1.2 and Na(v)1.6 are both normally expressed along premyelinated and myelinated axons at different stages of maturation and are also expressed in a subset of demyelinated axons, where coexpression of Na(v)1.6 together with the Na(+)/Ca(2+) exchanger is associated with axonal injury. It has been difficult to distinguish the currents produced by Na(v)1.2 and Na(v)1.6 in native neurones, and previous studies have not compared these channels within neuronal expression systems. In this study, we have characterized and directly compared Na(v)1.2 and Na(v)1.6 in a mammalian neuronal cell background and demonstrate differences in their properties that may affect neuronal behaviour. The Na(v)1.2 channel displays more depolarized activation and availability properties that may permit conduction of action potentials, even with depolarization. However, Na(v)1.2 channels show a greater accumulation of inactivation at higher frequencies of stimulation (20-100 Hz) than Na(v)1.6 and thus are likely to generate lower frequencies of firing. Na(v)1.6 channels produce a larger persistent current that may play a role in triggering reverse Na(+)/Ca(2+) exchange, which can injure demyelinated axons where Na(v)1.6 and the Na(+)/Ca(2+) exchanger are colocalized, while selective expression of Na(v)1.2 may support action potential electrogenesis, at least at lower frequencies, while producing a smaller persistent current.

MeSH Terms
Action Potentials/physiology Animals Axons/physiology Cells, Cultured Ganglia, Spinal/cytology,physiology Ion Channel Gating/physiology Male Membrane Potentials/physiology Mice NAV1.2 Voltage-Gated Sodium Channel NAV1.6 Voltage-Gated Sodium Channel Nerve Tissue Proteins/physiology Neurons, Afferent/physiology Recombinant Proteins/metabolism Sodium Channels/physiology
Chemicals
NAV1.2 Voltage-Gated Sodium Channel NAV1.6 Voltage-Gated Sodium Channel Nerve Tissue Proteins Recombinant Proteins Scn2a protein, mouse Scn8a protein, mouse Sodium Channels
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Rush Anthony M
Department of Neurology, Center for Neuroscience and Regeneration Research, Yale School of Medicine, LCI 707, 333 Cedar Street, New Haven, CT 06510, USA.
Dib-Hajj Sulayman D
Waxman Stephen G
References (45)
45 references, click to expand
  1. Ionic mechanisms of burst firing in dissociated Purkinje neurons.
    J Neurosci. 2003 Oct 22;23(29):9650-63 PMID: 14573545
  2. Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons.
    J Physiol. 2003 Sep 15;551(Pt 3):741-50 PMID: 12843211
  3. Co-localization of sodium channel Nav1.6 and the sodium-calcium exchanger at sites of axonal injury in the spinal cord in EAE.
    Brain. 2004 Feb;127(Pt 2):294-303 PMID: 14662515
  4. Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger.
    Proc Natl Acad Sci U S A. 2004 May 25;101(21):8168-73 PMID: 15148385
  5. Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice.
    J Neurophysiol. 2004 Aug;92(2):726-33 PMID: 15056687
  6. Resurgent Na currents in four classes of neurons of the cerebellum.
    J Neurophysiol. 2004 Nov;92(5):2831-43 PMID: 15212420
  7. Differential subcellular localization of the RI and RII Na+ channel subtypes in central neurons.
    Neuron. 1989 Dec;3(6):695-704 PMID: 2561976
  8. Anoxic injury of mammalian central white matter: decreased susceptibility in myelin-deficient optic nerve.
    Ann Neurol. 1990 Sep;28(3):335-40 PMID: 2241117
  9. Ionic mechanisms of anoxic injury in mammalian CNS white matter: role of Na+ channels and Na(+)-Ca2+ exchanger.
    J Neurosci. 1992 Feb;12(2):430-9 PMID: 1311030
  10. Three types of sodium channels in adult rat dorsal root ganglion neurons.
    Brain Res. 1992 Oct 2;592(1-2):283-97 PMID: 1280518
  11. Noninactivating, tetrodotoxin-sensitive Na+ conductance in rat optic nerve axons.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):6976-80 PMID: 8394004
  12. Characterization of TTX-sensitive and TTX-resistant sodium currents in small cells from adult rat dorsal root ganglia.
    J Physiol. 1993 Apr;463:39-56 PMID: 8246189
  13. Sodium channel mutations in paramyotonia congenita uncouple inactivation from activation.
    Neuron. 1994 Feb;12(2):281-94 PMID: 8110459
  14. Auxiliary subunits of voltage-gated ion channels.
    Neuron. 1994 Jun;12(6):1183-94 PMID: 7516685
  15. Structure and functional expression of a new member of the tetrodotoxin-sensitive voltage-activated sodium channel family from human neuroendocrine cells.
    EMBO J. 1995 Mar 15;14(6):1084-90 PMID: 7720699
  16. Spinal sensory neurons express multiple sodium channel alpha-subunit mRNAs.
    Brain Res Mol Brain Res. 1996 Dec 31;43(1-2):117-31 PMID: 9037525
  17. Low-threshold, persistent sodium current in rat large dorsal root ganglion neurons in culture.
    J Neurophysiol. 1997 Mar;77(3):1503-13 PMID: 9084615
  18. Downregulation of tetrodotoxin-resistant sodium currents and upregulation of a rapidly repriming tetrodotoxin-sensitive sodium current in small spinal sensory neurons after nerve injury.
    J Neurosci. 1997 May 15;17(10):3503-14 PMID: 9133375
  19. Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons.
    J Neurosci. 1997 Jun 15;17(12):4517-26 PMID: 9169512
  20. Persistent sodium currents through brain sodium channels induced by G protein betagamma subunits.
    Neuron. 1997 Aug;19(2):443-52 PMID: 9292732
  21. Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice.
    Neuron. 1997 Oct;19(4):881-91 PMID: 9354334
  22. Functional analysis of the mouse Scn8a sodium channel.
    J Neurosci. 1998 Aug 15;18(16):6093-102 PMID: 9698304
  23. Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia.
    J Physiol. 1998 Sep 15;511 ( Pt 3):771-89 PMID: 9714859
  24. Slow closed-state inactivation: a novel mechanism underlying ramp currents in cells expressing the hNE/PN1 sodium channel.
    J Neurosci. 1998 Dec 1;18(23):9607-19 PMID: 9822722
  25. Characterization of the isoform-specific differences in the gating of neuronal and muscle sodium channels.
    Can J Physiol Pharmacol. 1998 Oct-Nov;76(10-11):1041-50 PMID: 10100887
  26. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways.
    Nat Neurosci. 1999 Jun;2(6):541-8 PMID: 10448219
  27. Use-dependent potentiation of the Nav1.6 sodium channel.
    Biophys J. 2004 Dec;87(6):3862-72 PMID: 15465873
  28. Open-channel block by the cytoplasmic tail of sodium channel beta4 as a mechanism for resurgent sodium current.
    Neuron. 2005 Jan 20;45(2):233-44 PMID: 15664175
  29. Optimized protocol for biolistic transfection of brain slices and dissociated cultured neurons with a hand-held gene gun.
    J Neurosci Methods. 1999 Oct 15;92(1-2):55-64 PMID: 10595703
  30. The absence of resurgent sodium current in mouse spinal neurons.
    Brain Res. 1999 Dec 4;849(1-2):162-8 PMID: 10592298
  31. A novel persistent tetrodotoxin-resistant sodium current in SNS-null and wild-type small primary sensory neurons.
    J Neurosci. 1999 Dec 15;19(24):RC43 PMID: 10594087
  32. Nomenclature of voltage-gated sodium channels.
    Neuron. 2000 Nov;28(2):365-8 PMID: 11144347
  33. Electrophysiological and pharmacological properties of the human brain type IIA Na+ channel expressed in a stable mammalian cell line.
    Pflugers Arch. 2001 Jan;441(4):425-33 PMID: 11212204
  34. A gain-of-function mutation in the sodium channel gene Scn2a results in seizures and behavioral abnormalities.
    Neuroscience. 2001;102(2):307-17 PMID: 11166117
  35. Differential control of clustering of the sodium channels Na(v)1.2 and Na(v)1.6 at developing CNS nodes of Ranvier.
    Neuron. 2001 Apr;30(1):105-19 PMID: 11343648
  36. Compact myelin dictates the differential targeting of two sodium channel isoforms in the same axon.
    Neuron. 2001 Apr;30(1):91-104 PMID: 11343647
  37. Nav1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons.
    J Neurosci. 2001 Aug 15;21(16):5952-61 PMID: 11487618
  38. Sodium currents of large (Abeta-type) adult cutaneous afferent dorsal root ganglion neurons display rapid recovery from inactivation before and after axotomy.
    Neuroscience. 2001;106(1):161-9 PMID: 11564426
  39. A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar purkinje neurons.
    J Neurosci. 2002 Apr 15;22(8):3100-7 PMID: 11943813
  40. Molecular cloning, distribution and functional analysis of the NA(V)1.6. Voltage-gated sodium channel from human brain.
    Brain Res Mol Brain Res. 2002 Jun 30;103(1-2):80-90 PMID: 12106694
  41. Sodium channel Na(v)1.6 is expressed along nonmyelinated axons and it contributes to conduction.
    Brain Res Mol Brain Res. 2002 Sep 30;105(1-2):19-28 PMID: 12399104
  42. Abnormal sodium channel distribution in optic nerve axons in a model of inflammatory demyelination.
    Brain. 2003 Jul;126(Pt 7):1552-61 PMID: 12805113
  43. The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study.
    J Neurosci. 2003 Jun 15;23(12):4899-912 PMID: 12832512
  44. Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2.
    J Neurosci. 2003 Aug 20;23(20):7577-85 PMID: 12930796
  45. Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with beta-pompilidotoxin.
    J Neurosci. 2004 Jan 7;24(1):35-42 PMID: 14715935
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2005-05-01
Epub
2005-00-10
Pages
803-15
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1464456
Subset
IM
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