Characteristics of Na<sup>+</sup> current in Schwann cells cultured from frog sciatic nerve

Miyazaki, Toshihisa; Tasaka, Junko; Sakai, Saeko; Hashiguchi, Takashi; Padjen, Ante L.; Tosaka, Tsuneo

doi:10.1002/glia.440100406

Cited by 5 publications

(4 citation statements)

References 44 publications

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“…1.5 μm 2 and 3.0 μm 2 , respectively, implying a conductance density ( G per membrane area ) of 5.5 pS μm −2 and 5.0 pS μm −2 in the callosal and cerebellar internodal membranes, respectively. These values are similar to the previously reported specific conductance of 5.7 pS μm −2 for cultured Schwann cells from the frog sciatic nerve (Miyazaki et al 1994) and of 1.4 pS μm −2 for the non‐endfoot region of salamander retinal Müller glia (Newman, 1985).…”

Section: Resultssupporting

confidence: 90%

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Bakiri

Káradóttir

Cossell

et al. 2011

The Journal of Physiology

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Non-technical summary In the central nervous system, electrical signals passing along nerve cells are speeded by cells called oligodendrocytes, which wrap the nerve cells with a fatty layer called myelin. This layer is important for rapid information processing, and is often lost in disease, causing mental or physical impairment in multiple sclerosis, stroke, cerebral palsy and spinal cord injury. The myelin speeds the information flow in two ways, by decreasing the capacitance of the nerve cell and by increasing its membrane resistance, but little is known about the latter aspect of myelin function. By recording electrically from oligodendrocytes and imaging their morphology we characterised the geometry and, for the first time, the resistance of myelin in the brain. This revealed differences between the properties of oligodendrocytes in two brain areas and established that the resistance of myelin is sufficiently high to prevent significant slowing of the nerve electrical signal by current leakage through the myelin.Abstract Despite the textbook description that oligodendrocytes 'insulate' axons, the resistivity of the oligodendrocyte internodal membrane is unknown, and it is unknown how the electrical properties differ for oligodendrocytes which myelinate different numbers of axons or are located in different brain areas. We used whole-cell patch-clamping and dye-fill morphology to characterize the electrical properties of oligodendrocytes in the corpus callosum and the white matter of the cerebellum. At postnatal day 12, oligodendrocytes in the corpus callosum myelinated ∼10 axons, while oligodendrocytes in the cerebellum myelinated ∼7 axons. Internode lengths were shorter in the corpus callosum than in cerebellum, while the somata diameters of corpus callosal and cerebellar oligodendrocytes were similar. By correlating the conductance of the oligodendrocytes with the number and length of the internodes they made, we estimated the conductance of each internodal process and the conductivity per unit area of the oligodendrocyte internodal membrane. The derived resistance of one internodal process was ∼1.5 G in corpus callosal oligodendrocytes and ∼0.6 G in cerebellar oligodendrocytes. The specific conductance (depending on the assumptions made) was 0.63-5.5 pS μm −2 for corpus callosal oligodendrocytes and 0.28-5.0 pS μm −2 for cerebellar oligodendrocytes. These values were used, in a computational model of action potential propagation in a myelinated axon, to assess the effect of the oligodendrocyte conductance and anatomical parameters on the speed of action potential propagation. The measured oligodendrocyte membrane conductivity did Y. Bakiri and R. Káradóttir made an equal contribution. not significantly lower the action potential speed by short circuiting the myelin capacitance. Differences in axon diameter, number of myelin wraps and internode length predict that, other factors being equal, the conduction speed for cerebellar axons will be twice that for corpus callosal axons.

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Section: Resultssupporting

confidence: 90%

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Bakiri

Káradóttir

Cossell

et al. 2011

The Journal of Physiology

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“…Na + currents, albeit TTX‐sensitive ones, have been described in Schwann cells from rat and rabbit (Shrager et al . 1985; Chiu 1987), human (Konishi 1989a) and frog (Miyazaki et al . 1994), but not in mouse (Konishi 1989b; Hoppe et al .…”

Section: Discussionmentioning

confidence: 99%

“…The Na ϩ currents were resistant to TTX at 1 µM, and blocked by 5 mM Co 2ϩ , characteristics of 'TTX-resistant' Na ϩ currents (Ikeda & Schofield, 1987;Roy & Narahashi, 1992). Na ϩ currents, albeit TTX-sensitive ones, have been described in Schwann cells from rat and rabbit (Shrager et al, 1985;Chiu, 1987), human (Konishi, 1989a) and frog (Miyazaki et al, 1994), but not in mouse (Konishi, 1989b;Hoppe et al, 1989). TTX-resistant Na ϩ currents have been described in several cell types, including astrocytes (see Sontheimer & Ritchie, 1995) and DRG neurons (Roy & Narahashi, 1992;Cummins & Waxman, 1997).…”

Section: Na ϩ Currentsmentioning

confidence: 96%

Functional Ca²⁺ and Na⁺ channels on mouse Schwann cells cultured in serum‐free medium: regulation by a diffusible factor from neurons and by cAMP

Beaudu-Lange

Despeyroux

Marcaggi

et al. 1998

Eur J of Neuroscience

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Regulation of expression of functional voltage-gated ion channels for inward currents was studied in Schwann cells in organotypic cultures of dorsal root ganglia from E19 mouse embryos maintained in serum-free medium. Of the Schwann cells that did not contact axons, 46.5% expressed T-type Ca2+ conductances (ICaT). Two days or more after excision of the ganglia, and consequent disappearance of neurites, ICaT were detectable in only 10.9% of the cells, and the marker 04 disappeared. On Schwann cells deprived of neurons, T- (but not L-) type Ca2+ conductances were re-induced by weakly hydrolysable analogues of cAMP, and by forskolin (an activator of adenylyl cyclase) after long-term treatment (4 days). With CPT cAMP (0.1-2 mM), 8Br cAMP, db cAMP or forskolin (0.01 or 0.1 mM), the proportion of cells with ICaT was not significantly different from the proportion in the cultures with neurons. These agents also induced expression in some cells of tetrodotoxin-resistant Na+ currents, which were rarely induced by neurons, but 04 was not re-induced by cAMP analogue treatments that re-induced ICaT. Inward currents (Ba2+ or Na+) were partly restored (P < 0.05) on Schwann cells cultured for 6-7 days beneath a filter bearing cultured neurons. In contrast, addition of neuron-conditioned medium was ineffective. The results suggest that neurons activate, via diffusible and degradable factors, a subset of Schwann cell cAMP pathways leading to expression of IcaT, and activate additional non-cAMP pathways that lead to expression of 04.

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“…Boudier, unpublished results) that could be accounted for by an increase in the number of Schwann cells and the extension of Schwann cell processes (Lubischer and Thompson, 1999). Previous studies have already reported the presence of tetrodotoxin‐sensitive sodium currents in Schwann cell cultures derived from rabbit, rat, and frog sciatic nerves (Shrager et al, 1985; Miyazaki et al, 1994), or from mouse dorsal root ganglia (Beaudu‐Lange et al, 1998). Using excised patches, Chiu (1993) recorded sodium currents in freshly isolated Schwann cells from 10‐week‐old rabbit sciatic nerve.…”

Section: Discussionmentioning

confidence: 98%

Expression of Nav1.6 sodium channels by Schwann cells at neuromuscular junctions: Role in the motor endplate disease phenotype

Musarella¹,

Alcaraz²,

Caillol³

et al. 2005

Glia

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In addition to their role in action potential generation and fast synaptic transmission in neurons, voltage-dependent sodium channels can also be active in glia. Terminal Schwann cells (TSCs) wrap around the nerve terminal arborization at the neuromuscular junction, which they contribute to shape during development and in the postdenervation processes. Using fluorescent in situ hybridization (FISH), immunofluorescence, and confocal microscopy, we detected the neuronal Nav1.6 sodium channel transcripts and proteins in TSCs in normal adult rats and mice. Nav1.6 protein co-localized with the Schwann cell marker S-100 but was not detected in the SV2-positive nerve terminals. The med phenotype in mice is due to a mutation in the SCN8A gene resulting in loss of Nav1.6 expression. It leads to early onset in postnatal life of defects in neuromuscular transmission with minimal alteration of axonal conduction. Strikingly, in mutant mice, the nonmyelinated pre-terminal region of axons showed abundant sprouting at neuromuscular junctions, and most of the alpha-bungarotoxin-labeled endplates were devoid of S-100- or GFAP-positive TSCs. Using specific antibodies against the Nav1.2 and Nav1.6 sodium channels, ankyrin G and Caspr 1, and a pan sodium channel antibody, we found that a similar proportion of ankyrin G-positive nodes of Ranvier express sodium channels in mutant and wild-type animals and that nodal expression of Nav1.2 persists in med mice. Our data supports the hypothesis that the lack of expression of Nav1.6 in Schwann cells at neuromuscular junctions might play a role in the med phenotype.

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Characteristics of Na⁺ current in Schwann cells cultured from frog sciatic nerve

Cited by 5 publications

References 44 publications

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Functional Ca²⁺ and Na⁺ channels on mouse Schwann cells cultured in serum‐free medium: regulation by a diffusible factor from neurons and by cAMP

Expression of Nav1.6 sodium channels by Schwann cells at neuromuscular junctions: Role in the motor endplate disease phenotype

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Characteristics of Na+ current in Schwann cells cultured from frog sciatic nerve

Cited by 5 publications

References 44 publications

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Morphological and electrical properties of oligodendrocytes in the white matter of the corpus callosum and cerebellum

Functional Ca2+ and Na+ channels on mouse Schwann cells cultured in serum‐free medium: regulation by a diffusible factor from neurons and by cAMP

Expression of Nav1.6 sodium channels by Schwann cells at neuromuscular junctions: Role in the motor endplate disease phenotype

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Characteristics of Na⁺ current in Schwann cells cultured from frog sciatic nerve

Functional Ca²⁺ and Na⁺ channels on mouse Schwann cells cultured in serum‐free medium: regulation by a diffusible factor from neurons and by cAMP