Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent

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Abstract

The whole-cell configuration of the patch-clamp technique, immunoprecipitation experiments and unilateral naris occlusions were used to investigate whether the voltage-gated potassium channel Kv1.3 was a substrate for neurotrophin-induced tyrosine phosphorylation and subsequent functional modulation of current properties in cultured rat olfactory bulb (OB) neurons. Membrane proteins of the OB included all three Trk receptor kinases, but the truncated form of the receptor, lacking an intact kinase domain, was the predominant form of the protein for TrkA and TrkC, while TrkB was predominantly found as the full-length receptor. Acute (15 min) stimulation of OB neurons with bath application of 50 ng ml-1 brain-derived neurotrophic factor (BDNF), which is a selective ligand for TrkB, caused suppression of the whole-cell outward current and no changes in the kinetics of inactivation or deactivation. Acute stimulation with either nerve growth factor or neurotrophin-3 failed to evoke any changes in Kv1.3 function in the OB neurons. Chronic exposure to BDNF (days) caused an increase in the magnitude of Kv1.3 current and speeding of the inactivation and deactivation of the channel. Acute BDNF-induced activation of TAB receptors significantly increased tyrosine phosphorylation of Kv1.3 in the OB, as shown using a combined immunoprecipitation and Western blot analysis. With unilateral naris occlusion, the acute BDNF-induced tyrosine phosphorylation of Kv1.3 was increased in neurons lacking odour sensory experience. In summary, the duration of neurotrophin exposure and the sensory-dependent state of a neuron can influence the degree of phosphorylation of a voltage-gated ion channel and its concomitant functional modulation by neurotrophins.

Original languageEnglish (US)
Pages (from-to)413-429
Number of pages17
JournalJournal of Physiology
Volume542
Issue number2
DOIs
StatePublished - Jul 15 2002

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trkB Receptor
Voltage-Gated Potassium Channels
Olfactory Bulb
Nerve Growth Factors
Brain-Derived Neurotrophic Factor
Neurons
Phosphorylation
Tyrosine
Immunoprecipitation
trkC Receptor
Phosphotransferases
Neurotrophin 3
Patch-Clamp Techniques
Nerve Growth Factor
Baths
Ion Channels
Membrane Proteins
Western Blotting
Ligands

All Science Journal Classification (ASJC) codes

  • Physiology

Cite this

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title = "Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent",
abstract = "The whole-cell configuration of the patch-clamp technique, immunoprecipitation experiments and unilateral naris occlusions were used to investigate whether the voltage-gated potassium channel Kv1.3 was a substrate for neurotrophin-induced tyrosine phosphorylation and subsequent functional modulation of current properties in cultured rat olfactory bulb (OB) neurons. Membrane proteins of the OB included all three Trk receptor kinases, but the truncated form of the receptor, lacking an intact kinase domain, was the predominant form of the protein for TrkA and TrkC, while TrkB was predominantly found as the full-length receptor. Acute (15 min) stimulation of OB neurons with bath application of 50 ng ml-1 brain-derived neurotrophic factor (BDNF), which is a selective ligand for TrkB, caused suppression of the whole-cell outward current and no changes in the kinetics of inactivation or deactivation. Acute stimulation with either nerve growth factor or neurotrophin-3 failed to evoke any changes in Kv1.3 function in the OB neurons. Chronic exposure to BDNF (days) caused an increase in the magnitude of Kv1.3 current and speeding of the inactivation and deactivation of the channel. Acute BDNF-induced activation of TAB receptors significantly increased tyrosine phosphorylation of Kv1.3 in the OB, as shown using a combined immunoprecipitation and Western blot analysis. With unilateral naris occlusion, the acute BDNF-induced tyrosine phosphorylation of Kv1.3 was increased in neurons lacking odour sensory experience. In summary, the duration of neurotrophin exposure and the sensory-dependent state of a neuron can influence the degree of phosphorylation of a voltage-gated ion channel and its concomitant functional modulation by neurotrophins.",
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Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. / Tucker, Kristal Raylone; Fadool, D. A.

In: Journal of Physiology, Vol. 542, No. 2, 15.07.2002, p. 413-429.

Research output: Contribution to journalArticle

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AU - Tucker, Kristal Raylone

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