Potassium channel regulation in Schwann cells during early developmental myelinogenesis

Wilson, Gisela F.; Chiu, Shing Yan

doi:10.1523/jneurosci.10-05-01615.1990

Cited by 61 publications

(74 citation statements)

References 23 publications

(43 reference statements)

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“…During development, Kv1.1 is expressed in undifferentiated glia in the mouse embryo (47) and in isolated sciatic nerve in early postnatal rats (48). At the electrophysiological level, a sustained outward K ϩ current is downregulated during Schwann cell differentiation (49). In addition, 24-72 h of incubation of cultured oligodendrocytes with tumor necrosis factor-␣ has been shown to elevate intracellular cAMP levels, leading to a subsequent down-regulation of an outwardly rectifying K ϩ current and a decrease in the RMP (50).…”

Section: Discussionmentioning

confidence: 99%

Cyclic AMP regulates potassium channel expression in C6 glioma by destabilizing Kv1.1 mRNA

Allen

Koh

Tempel

1998

Proc. Natl. Acad. Sci. U.S.A.

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The tissue distributions and physiological properties of a variety of cloned voltage-gated potassium channel genes have been characterized extensively, yet relatively little is known about the mechanisms controlling expression of these genes. Here, we report studies on the regulation of Kv1.1 expressed endogenously in the C6 glioma cell line. We demonstrate that elevation of intracellular cAMP leads to the accelerated degradation of Kv1.1 RNA. The cAMP-induced decrease in Kv1.1 RNA is followed by a decrease in Kv1.1 protein and a decrease in the whole cell sustained K ؉ current amplitude. Dendrotoxin-I, a relatively specific blocker of Kv1.1, blocks 96% of the sustained K ؉ current in glioma cells, causing a shift in the resting membrane potential from ؊40 mV to ؊7 mV. These data suggest that expression of Kv1.1 contributes to setting the resting membrane potential in undifferentiated glioma cells. We therefore suggest that receptor-mediated elevation of cAMP reduces outward K ؉ current density by acting at the translational level to destabilize Kv1.1 RNA, an additional mechanism for regulating potassium channel gene expression.Regulation of gene expression can occur at the level of transcription, translation, or posttranslationally. Among the genes encoding voltage-gated potassium (Kv) channels, transcriptional regulation has been analyzed for Kv1.5 and Kv3.1 (1-5). For example, Takimoto et al. (6) demonstrated that expression levels of Kv1.5 were affected at the level of transcription with dexamethasone treatment but that mRNA halflife and protein turnover were unchanged. Posttranslational regulation has also been convincingly demonstrated for a number of Kv channels. For example, phosphorylation by tyrosine kinase, protein kinase C, and protein kinase A have each been shown to modulate Kv channel function (7-9), and a channel-associated ␤-subunit (Kv␤2) has been shown to promote translocation of Kv1.2 to the plasma membrane (10). In contrast, relatively little is known about regulation of Kv genes at the translational level. Given the fact that many Kv transcripts are large (6-12 kb) but contain relatively small ORFs (1.5-2.5 kb), it seems likely that the untranslated portions of these transcripts may have a regulatory function.There exists a variety of forms of translational regulation, including changes in nuclear processing of the transcript (splicing, capping, polyadenylation, and nuclear export) as well as changes in the efficiency of translation (ribosome binding, loading, scanning, and initiation) and changes in transcript stability (reviewed in ref. 11). Well studied examples include S-adenosylmethionine decarboxylase, regulated by changing the efficiency of ribosome loading and scanning (12), and iron metabolism, regulated by blockade of ribosome scanning and by regulation of transcript stability in the ferritin and transferrin receptor genes, respectively (13). Among ion channel genes, Wymore et al. (14) demonstrated that alternatively spliced 3Ј-untranslated regions (UTRs) from Kv1.4 caus...

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Section: Discussionmentioning

confidence: 99%

Cyclic AMP regulates potassium channel expression in C6 glioma by destabilizing Kv1.1 mRNA

Allen

Koh

Tempel

1998

Proc. Natl. Acad. Sci. U.S.A.

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“…Electrophysiological experiments were performed using a Nikon Diaphot inverted microscope equipped with epifluorescent optics for viewing dye-stained cells. Patch-clamp studies were carried out as described previously (Wilson and Chiu, 1990). Briefly, using a List EPC-7 amplifier, recordings were made on myelinated nerve fibers 1-8 hr after isolation.…”

Section: Methodsmentioning

confidence: 99%

“…Previous patch-clamp experiments on myelinating Schwann cells were restricted to the cell soma (Chiu, 1987(Chiu, , 1988. Interestingly, these studies have shown that channels are present only transiently during early development and disappear from the soma as the animal matures (Wilson and Chiu, 1990). However, the possibility of a regional specialization in ion channels in the paranodal region cannot be excluded.…”

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confidence: 99%

Ion channels in axon and Schwann cell membranes at paranodes of mammalian myelinated fibers studied with patch clamp

1990

J. Neurosci.

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While recent studies have established the presence of voltage-gated ion channels on Schwann cells in culture and on freshly isolated fibers from mature mammals, an important issue not yet explored is whether Schwann cell channels are regionally specialized. In the nodal region, the intimate association between the Schwann cell and its axon suggests that this is a likely site for functional specialization. Here, we examine whether there is a localized expression of channels in the Schwann cell paranodal regions, in a manner similar to that already shown for the nodal axon. Cell-attached and outside-out patch-clamp recordings were made from paranodal regions of rat myelinated sciatic nerve fibers where the myelin on both sides of the node was retracted by enzymatic treatment. Even though no myelin was visible on the surface of the retracted paranode, significant portions of this surface were found to stain positively with a marker (anti-galactocerebroside) for Schwann cell membranes, suggesting that part of the axon still was covered by glial membranes. Using Lucifer yellow in the recording pipettes, we observed that the dye diffused into either axons or Schwann cells when the membrane under the tip was ruptured. Using this as a criterion to identify membranes obtained from retracted paranodes, we found delayed and inwardly rectifying potassium channels on both axon- and Schwann-derived patches. However, sodium channels were detected only in axon patches. This is the first report that voltage- gated glial channels are present in immediate vicinity to axons of the PNS. This finding, coupled with earlier reports that functional channels are absent in soma of mature myelinating Schwann cells, suggests that ion channels in these cells are regionally specialized for functional interaction with axons.

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“…Fish oligodendrocyte-like cells resemble in several respects to mammalian Schwann cells. They show little current responses like myelinating Schwann cells or outward rectification like non-myelinating Schwann cells (Chiu 1988;Wilson and Chiu 1990) and lack pH-and glutamate activated currents. Furthermore they heavily proliferate in culture, another property that these cells share with mammalian Schwann cells.…”

Section: Discussionmentioning

confidence: 99%

Two populations of glial cells from fish optic nerve/tract with distinct electrophysiological properties

et al. 1991

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Summary.The electrophysiological properties of the two major glial cell types in cultures from the regenerating goldfish optic nerve/tract were studied with patch-clamp techniques. Spindle-shaped cells express myelin proteins. These oligodendrocyte-like cells possess outwardly rectifying currents, do not show glutamate activated currents and are rarely electrically coupled to neighboring cells. Cells of epitheloid morphology probably represent astrocytes. They are GFAP-positive and do not exhibit myelin proteins. These cells have glutamate activated currents, display a linear current to voltage relationship and are extensively electrically coupled thus displaying properties similar to mammalian astrocytes.

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Potassium channel regulation in Schwann cells during early developmental myelinogenesis

Cited by 61 publications

References 23 publications

Cyclic AMP regulates potassium channel expression in C6 glioma by destabilizing Kv1.1 mRNA

Cyclic AMP regulates potassium channel expression in C6 glioma by destabilizing Kv1.1 mRNA

Ion channels in axon and Schwann cell membranes at paranodes of mammalian myelinated fibers studied with patch clamp

Two populations of glial cells from fish optic nerve/tract with distinct electrophysiological properties

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