Ionic currents in the somatic membrane of rat dorsal root ganglion neurons —III. Potassium currents

Kostyuk, P. G.; Veselovsky, N.S.; Fedulova, S. A.; Tsyndrenko, A. Ya.

doi:10.1016/0306-4522(81)90090-7

Cited by 70 publications

(35 citation statements)

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“…Small DRG neurons (Ϸ20 m) typically display a variable combination of rapidly inactivating A-type (I A ), slowly inactivating, and sustained components of K ϩ current (Kostyuk et al, 1981). Figure 1A shows the whole-cell current of a DRG neuron expressing all three of these currents.…”

Section: Resultsmentioning

confidence: 99%

“…BAB is an inhibitor of the sodium, calcium, and delayed rectifier potassium currents of DRG neurons (Van den Berg et al, 1996;Beekwilder et al, 2003Beekwilder et al, , 2005, suggesting that the reduced electrical excitability of dorsal root pain fibers is the most likely mechanism of BAB anesthesia ( Van den Berg et al, 1995). Electrophysiological characterization of small DRG neurons has identified three broad classifications of voltage-gated K ϩ current expressed in these cells: a fast-inactivating ( Ϸ 10-ms) 4-aminopyridine (4-AP)-sensitive A-type current (I A ), a slowly inactivating ( Ϸ 100-ms) current, and a tetraethylammonium (TEA)-sensitive sustained current (Kostyuk et al, 1981;Christian et al, 1994;Gold et al, 1996;Safronov et al, 1996;Fedulova et al, 1998;Yoshimura and de Groat, 1999;Sculptoreanu et al, 2004).…”

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Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

Winkelman¹,

Beck²,

Ypey³

et al. 2005

J Pharmacol Exp Ther

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n-Butyl-p-aminobenzoate (BAB; butamben) is a long-duration anesthetic used for the treatment of chronic pain. Epidural administration of BAB is thought to reduce the electrical excitability of dorsal root nociceptor fibers by inhibiting voltagegated ion channels. To further investigate this mechanism, we examined the effects of BAB on the potassium currents of acutely dissociated neurons from the rat dorsal root ganglion (DRG). These neurons express a rapidly inactivating A-type K ϩ current (I A ) that is resistant to tetraethylammonium (20 mM) but inhibited by 4-aminopyridine (5 mM). At low concentrations, BAB (Յ1 M) selectively inhibited the I A component of DRG K ϩ current. The voltage dependence of activation and inactivation, kinetics of recovery from inactivation, and the pharmacology of the DRG I A were similar to those of the Kv4 family of K ϩ channels. Reverse transcription-polymerase chain reaction was used to establish that the messages encoding for all three of the mammalian Kv4 channel subunits (Kv4.1-Kv4.3) were present in the rat DRG. BAB produced a high-affinity, partial inhibition of heterologously expressed Kv4.2 channels (K D ϭ 59 nM) but did not alter the kinetics or voltage sensitivity of gating. Substituting polar threonines for conserved hydrophobic residues of the S6 segment weakened BAB binding but did not alter the voltage-dependent gating of the Kv4.2 channel. At physiological pH, BAB is uncharged, suggesting that hydrophobic interactions may contribute to drug binding. The data support a mechanism in which BAB binds near the narrow cytoplasmic entrance of Kv4 channels and inhibits current by a pore blocking mechanism.

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

Winkelman¹,

Beck²,

Ypey³

et al. 2005

J Pharmacol Exp Ther

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“…The classical and more accurate method for estimating the reversal potential of a voltage sensitive conductance, i.e. tail current reversal, could not be usefully applied in this case due to the activation of several outward rectifiers in the membrane potential range over which reversal was expected (M. L. Mayer & G. L. Westbrook, unpublished observations; see also Kostyuk, Veselovsky, Fedulova & Tsyndrenko, 1981 Gh activation curve The activation curve of Gh was estimated from the amplitude of the tail currents recorded at -50 or -60 mV following a series of hyperpolarizing prepulses. In ten neurones in which the tail current amplitude, normalized with respect to the maximum recorded, was plotted against the membrane potential during the hyperpolarizing prepulse, the data points were well fitted by activation curves generated by an equation of the form / V-\-…”

Section: Inward Rectification In Sensory Neurones 25mentioning

confidence: 99%

A voltage‐clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones.

Mayer

Westbrook

1983

The Journal of Physiology

426

320

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SUMMARY1. Mouse embryo dorsal root ganglion neurones were grown in tissue culture and voltage-clamped with two micro-electrodes. Hyperpolarizing voltage commands from holding potentials of -50 to -60 mV evoked slow inward current relaxations which were followed by inward tail currents on repolarization to the holding potential. These relaxations are due to the presence of a time-and voltage-dependent conductance provisionally termed Gh.2. Gh activates over the membrane potential range -60 to -120 mV. The presence of Gh causes time-dependent rectification in the current-voltage relationship measured between -60 and --120 mV. Gh does not inactivate within this range and thus generates a steady inward current at hyperpolarized membrane potentials.3. The current carried by Gh increases when the extracellular K+ concentration is raised, and is greatly reduced in Na+-free solutions. Current-voltage plots show considerably less inward rectification in Na+-free solution; conversely inward rectification is markedly enhanced when the extracellular K+ concentration is raised. The reversal potential of 'h is close to -30 mV in media of physiological composition.Tail-current measurement suggests that Ih is a mixed Na+-K+ current.4. Low concentrations ofCs+ reversibly block Ih and produce outward rectification in the steady-state current-voltage relationship recorded between membrane potentials of -60 and -120 mV. Cs+ also reversibly abolishes the sag and depolarizing overshoot that distort hyperpolarizing electrotonic potentials recorded in currentclamp experiments.5. Impermeant anion substitutes reversibly block Ih; this block is different from that produced by Cs+ or Na+-free solutions: Cs+ produces outward rectification in the steady-state current-voltage relationship recorded over the Ih activation range; in Na+-free solutions inward rectification, of reduced amplitude, can still be recorded since Ih is a mixed Na+-K+ current; in anion-substituted solutions the current-voltage relationship becomes approximately linear.6. It is concluded that in dorsal root ganglion neurones anomalous rectification is generated by the time-and voltage-dependent current Ih. The possible function of Ih in sensory neurones is discussed.

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“…Kv currents in sensory neurons are divided into two major categories: sustained, delayed rectifier-type K ϩ (K DR ) and transient A-type K ϩ (K A ) currents (Gold et al 1996;Hall et al 1994;Kostyuk et al 1981;Yoshimura et al 1996). K A currents in DRG cells consist of at least two different components, based on their inactivation kinetics (i.e., fast-and slow-inactivating K A currents) (Akins and McCleskey 1993;Everill et al 1998;McFarlane and Cooper 1991).…”

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Differential contribution of Kv4-containing channels to A-type, voltage-gated potassium currents in somatic and visceral dorsal root ganglion neurons

Yunoki

Takimoto

Kita

et al. 2014

Journal of Neurophysiology

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Ionic currents in the somatic membrane of rat dorsal root ganglion neurons —III. Potassium currents

Cited by 70 publications

References 10 publications

Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

A voltage‐clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones.

Differential contribution of Kv4-containing channels to A-type, voltage-gated potassium currents in somatic and visceral dorsal root ganglion neurons

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Ionic currents in the somatic membrane of rat dorsal root ganglion neurons —III. Potassium currents

Cited by 70 publications

References 10 publications

Inhibition of the A-Type K+Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

Inhibition of the A-Type K+Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

A voltage‐clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones.

Differential contribution of Kv4-containing channels to A-type, voltage-gated potassium currents in somatic and visceral dorsal root ganglion neurons

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Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben

Inhibition of the A-Type K⁺Channels of Dorsal Root Ganglion Neurons by the Long-Duration Anesthetic Butamben