Four Voltage-Gated Potassium Currents in Trigeminal Root

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Four Voltage-Gated Potassium Currents in Trigeminal Root

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International Journal of Oral Bioiogy, Vol. 38, No. 1 March 31 2013, p. 13-19 Copyright ⓒ 2013, The Korean Academy of Oral Bioiogy
http://dx.doi.org/10.11620/IJOB.2013.38.1.013

Four Voltage-Gated Potassium Currents in Trigeminal Root Ganglion Neurons
Seung Ho Choi1, Chang Youn1, Ji-Il Park2, Soon-Yeon Jeong1, Won-Man Oh1, Ji-Yeon Jung1, and Won-Jae Kim1* 1Dental Science Research Institute, School of Dentistry, Research Center for Biomineralization Disorder, Chonnam National University 2Department of Dental Hygiene, Gwangju Health University, Gwangju 500-757, Korea
(received Feburary 5, 2013 ; revised March 7, 2013 ; accepted March 8, 2013)

Various voltage-gated K+ currents were recently described in dorsal root ganglion (DRG) neurons. However, the characterization and diversity of voltage-gated K+ currents have not been well studied in trigeminal root ganglion (TRG) neurons, which are similar to the DRG neurons in terms of physiological roles and anatomy. This study was aimed to investigate the characteristics and diversity of voltage-gated K+ currents in acutely isolated TRG neurons of rat using whole cell patch clamp techniques. The first type (type I) had a rapid, transient outward current (IA) with the largest current size having a slow inactivation rate and a sustained delayed rectifier outward current (IK) that was small in size having a fast inactivation rate. The IA currents of this type were mostly blocked by TEA and 4-AP, K channel blockers whereas the IK current was inhibited by TEA but not by 4-AP. The second type had a large IA current with a slow inactivation rate and a medium size-sustained delayed IK current with a slow inactivation rate. In this second type (type II), the sensitivities of the IA or IK current by TEA and 4-AP were similar to those of the type I. The third type (type III) had a medium sized IA current with a fast inactivation rate and a large sustained IK current with the slow inactivation rate. In type III
*Correspondence to: Won Jae Kim, Dental Science Research Institute, School of Dentistry, Chonnam National University, 300 Yongbong-dong, Buk-gu, Gwangju 500-757, Korea, Tel: +8262-530-4881, Fax: +82-62-530-4885, E-mail: [email protected]
This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License(http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

current, TEA decreased both IA and IK but 4-AP only blocked IA current. The fourth type (type IV) had a smallest IA with a fast inactivation rate and a large IK current with a slow inactivation rate. TEA or 4-AP similarly decreased the IA but the IK was only blocked by 4-AP. These findings suggest that at least four different voltage-gated K+ currents in biophysical and pharmacological properties exist in the TRG neurons of rats.
Key words: Trigeminal root ganglion neurons, Voltagegated K+ currents
Introduction
Dorsal root ganglia (DRG) neurons transmit various sensory information such as touch, pressure, pain and temperature from the peripheral region to the CNS. Similarly, a pair of trigeminal root ganglia (TRG) is responsible for the sensory inputs from the oromaxillofacial region to which the trigeminal nerve is innervated.
TRG Primary afferent neurons are a functionally diverse population of neurons that transduce and encode a variety of stimuli. Some of this diversity may reflect a differential distribution of voltage-gated K+ currents, a class of currents that plays an integral role in the regulation of a number of neuronal response properties including spike repolarization, interspike interval, and burst adaptation [1]. In broad category, K+ currents carried by voltage-gated potassium channels are classified into 3 types; transient A type, delayed rectifier and in-

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Seung Ho Choi, Chang Youn, Ji-Il Park, Soon-Yeon Jeong, Won-Man Oh, Ji-Yeon Jung, and Won-Jae Kim

ward rectifier [2]. Although two [3], and subsequently three [4,5] distinct voltage-gated K+ currents have been identified in neurons from rat sensory ganglia, the steady-state and kinetic properties of these currents appear variable between studies. For an example, a slowly inactivating transient current (Atype K+ current) is present in sensory neurons that has an inactivation time constant that varies between 150 and 300 ms.
In addition, although many investigators have reported the existence of a single sustained delayed rectifier-type current in sensory neurons, a recent report by Akins and McCleskey (1993) suggests that some delayed rectifier-type current in dorsal root ganglion (DRG) neurons is subject to steady- state inactivation [6]. One explanation for the variability observed by these investigators is that there are more than three distinct voltage-gated K+ currents present in sensory neurons. In fact, six voltage-gated K+ currents were recently reported to be existed in DRG neurons [7]. However characterization and diversity of voltage-gated K currents have been not well known in TRG neurons, similar to the DRG neurons in physiological roles and anatomy. This study was aimed to investigate the diversity and characterization of voltagegated K+ currents in acutely isolated SD rat TRG neurons using whole cell patch clamp technique because the electrophysiological mechanisms that give rise to the diversity of response properties observed among sensory neurons requires a thorough knowledge of the properties of the currents expressed in those neurons.
Materials and Methods
Preparation of rat TRG neurons All experiments were carried out according to the guiding
principles for the care and use of animals approved by the ethics committee in Chonnam and Chosun University and the National Institutes of Health Guide for the care and Use of Laboratory Animals, and every effort was made to minimize both the number of animals used and their suffering. Rat TRG neurons were prepared by the method described previously [8]. After the decapitation of Sprague-Dawley rats (postnatal 7-14 days), a pair of trigeminal ganglia were dissected and washed several times in cold (4℃) dissociation solution containing (in mM) 140 NaCl, 5 KCl, 22 KH2PO4, 17 Na2HPO4, 5 Glucose, 59 Sucrose, pH 7.2. They were incubated at 37℃ for 40 min in dissociation solution and incu-

bated at 37℃ for 40 min in dissociation solution containing 1% trypsin. Then they were re-triturated and washed several times in modified MEM and maintained in 5% CO2 incubator (37℃). The isolated cells were used in electrophysiological recording within 3 hrs.
Electrophysiology Conventional whole cell voltage-clamp techniques were
used for electrophysiological recording. Patch pipettes were pulled on a Brown Flaming electrode puller (model p-87, Sutter instruments, USA) and forged using microforge (MF-83, Narishige, Japan). The pipette resistance ranged from 2-4 MΩ when filled with electrode solution (see below). The recording chamber was continuously perfused with bath solution (flow rate 0.5 ml/min). All experiments were done at room temperature (21-24℃).
The bath solution was composed of (in mM) 135 NaCl, 5 KCl, 1 MgCl2, 1.8 MnCl2, 5 Glucose, 10 HEPES, pH 7.4. The pipette solution contained (in mM) 10 NaCl, 140 KCl, 1 CaCl2, 1 MgCl2. 1 GTP, 5 ATP, 10 HEPES, 10 EGTA, pH 7.2. Both solution’s pH were adjusted with Tris-base. All components of the bath and electrode solutions were obtained from Sigma Co. The K+ channel blocking agents, 4-aminopyridine (4-AP) and Tetraethylammonium (TEA) were applied to the bath using superfusion method.
Data recording and analysis IK currents of TRG neurons were amplified using an Axo-
patch 200 B patch clamp amplifier (Axon instruments, USA), filtered at 1 kHz with an 80-dB/decade low-pass Bessel filter. Data analysis was facilitated by the use of commercially available software programs including pClamp 7 and Origin 4.1. The neuron diameter was measured with an eye piece micrometer under phase contrast illumination. Normalized peak conductances (G/Gmax) and the data describing the fractional decrease in the peak currents during the steadystate inactivation (I/Imax) were fitted with a Boltzmann function ; I/I max or G/Gmax = 1 + exp(V1/2- Vm)/k.
Results
Characterization of type I K+ current Type I K+ current was characterized as a whole current com-
posed of a large rapid, transient outward current (IA) having

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Table 1. Electrophysiological and pharmacological comparison of voltage-gated K+ currents in TRG neurons

Properties

I

II

III

IV

SS Inactivation (K1/2,mV)
SS Activation (K1/2,mV)

-68.3±2.8 -62.3±2.1 -60.7± -79.1±1.9 (n=11) (n=8) 2.2(n=10) (n=11)
-33.3±3.2 -28.7±1.7 -41.2± -26.9±2.9 (n=11) (n=8) 2.4(n=10) ( n=11)

TEA sensitivity

IA

++

++

+

-

Delayed IK

++

++

++

++

4-AP sensitivity

IA

+++

+++

+++

+++

Delayed IK

-

-

-

++

Prepulse (-30 mV) +

+

+

+

Prepulse (0 mV)

Activation time 16.4±1.1 7.9±0.9(n 17.7±0.9( 6.1±0.8(n constant (ms) (n=11) =8) n=10) =11)

I-V relation

R

R

R

R

IA size

L

L

M

S

IA Inactivation rate slow slow fast

Fast

Delayed K current S

M

L

L

size

Delayed K current fast inactivation rate

slow slow slow

Abbreviation: SS, steady-state; R, rectification; L, large; M,

medium; S, small

Fig. 1. Variability of the outward currents in different rat TRG neurons. Membrane potential held at -80 mV. The activation protocol consisted of 500ms or 1.5s depolarizing voltage steps to potentials ranging between -80 and +90 mV, after a 300 ms step to either -80, -30 and 0 mV.

Fig. 2. Electrophysiological properties of Type I K+ currents and effect of TEA and 4-AP on type I currents. A) The normalized peak currents vs. prepulse potential is plotted. The peak currents evoked from each prepulse potential in the steady-state inactivation protocol was normalized with respect to the peak current evoked from -120 mV(V1/2(inact) = -33.3±3.2 mV, n=11). Normalized peak conductance (G/Gmax) was fitted with a Boltzmann function (G/Gmax = 1 + exp(V1/2-Vm)/k, V1/2(act.) = -68.3±2.8 mV, n=11). B) Membrane voltage was held at -80 mV and stepped from -80 mV to 30 mV in 10 mV increment for 400 msec and held at -80 mV again. Sampling rate was 500 ㎲(2 kHz). The applicated concentrations of Tetraethylammonium (TEA) and 4-aminopyridine (4-AP) were indicated. 4-AP block selectively a transient component of the outward currents, sparing a sustained component while a transient current and sustained current were sensitive to the TEA.

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slow inactivation rate and a small delayed sustained outward current (IK) with fast inactivation rate (Table 1, Fig. 1 and 2). IA was isolated as the difference between the current evoked from a holding potential +80 mV and that evoked from a holding potential of -30 mV (Fig. 1). Type I IA was a relative large current that had the relative slow inactivation rate even though its activation rate is faster than type II.
Half-maximum activation and inactivation of IA were -33.3 mV and -68 mV (Table 1, Fig. 2). Activation time constant of IA showed an exponential dependence on membrane potential change e-fold in 16.6 mV. IK in type I was relatively small current with the fast inactivation rate. Type IA was mostly blocked TEA and 4-AP while IK was significantly inhibited by TEA but not by 4-AP (Table 1, Fig. 2).
Characterization of type II K+ current Type II K+ current was characterized as a whole current
composed of a large IA with slow inactivation and a relative medium size IK with slow inactivation rate (Table 1, Fig 1). Type II IA was a relatively large current which had relatively slow inactivation rate and blocked with -30 mV pre-pulse. Half-maximum activation and half-maximum steady-state
Fig. 3. Electrophysiological properties of Type II currents and effect of TEA and 4-AP on type II currents. A) Normalized peak currents (I/Imax) and normalized peak conductance (G/ Gmax) was fitted with a Boltzmann function (K1/2(act) = -28.7± 1.7 mV, K1/2(inact) = -62.3±2.1 mV, n=8). B) Membrane voltage was held at -80 mV and stepped from -80 mV to 30 mV in 10 mV increment for 400 msec and held at -80 mV again. Sampling rate was 500 ㎲(2 kHz). The applicated concentrations of Tetraethylammonium (TEA) and 4-aminopyridine (4-AP) were indicated. 4-AP block selectively a transient component of the outward currents, sparing a sustained component.

Fig. 4. Electrophysiological properties of Type III currents and effect of TEA and 4-AP on type III currents. A) Normalized peak currents (I/Imax) and normalized peak conductance (G/ Gmax) was fitted with a Boltzmann function (K1/2(act) = -41.2± 2.4 mV, K1/2(inact) = -60.7±2.2 mV, n=10). B) Membrane voltage was held at -80 mV and stepped from -80 mV to 30 mV in 10 mV increment for 400 msec and held at -80 mV again. Sampling rate was 500 ㎲(2 kHz). The applicated concentrations of Tetraethylammonium (TEA) and 4-aminopyridine (4-AP) were indicated. 4-AP blocked selectively a transient component of the outward currents, sparing a sustained component.
inactivation of IA were -28.7 and -62.3 mV (Table 1) Activation time constant showed an exponential dependence on membrane potential change e-fold in 14.7 mV (Table 1, Fig. 3). I-V relationship curve showed linear rectification and voltage dependency (Fig. 3).
IK was small and had slow inactivation rate. Sensitivities of TEA and 4-AP to the IA or IK were similar to those of the type ; 4-AP almost blocked IA but not IK whereas TEA significantly inhibited IA and IK (Table 1, Fig. 3).
Characterization of type III K+ current Type III K+ current was characterized as a medium IA with
slow inactivation rates and a large IK with fast inactivation rates (Table 1, Fig. 1 and 4). Type III IA was relatively medium size current and showed fast activation rate blocked by -30 mV pre-pulse. Half-maximum activation and half-maximum inactivation of IA were 41.2 mV and -60.7 mV. Activation time constant of IA showed an exponential dependence on membrane potential change e-fold in 9.46 mV. The IK was relatively large current with slow inactivation rates. Type III IA was completely blocked by 4-AP and partially inhibited by TEA whereas IK was only significantly blocked by TEA but not by 4-AP (Fig. 4).

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Fig. 5. Electrophysiological properties of Type IV currents and effect of TEA and 4-AP on type IV currents. A) Normalized peak currents (I/Imax) and normalized peak conductance (G/ Gmax) was fitted with a Boltzmann function (K1/2(act) = -26.9± 2.9 mV, K1/2(inact) = -79.1±1.9 mV, n=11). B) Membrane voltage was held at -80 mV and stepped from -80 mV to 30 mV in 10 mV increment for 400 msec and held at -80 mV again. Sampling rate was 500 ㎲(2 kHz). The applicated concentrations of Tetraethylammonium (TEA) and 4-aminopyridine (4-AP) were indicated. 4-AP blocked selectively a transient component of the outward currents, sparing a sustained component.
Characterization of type IV K+ current Type IV K+ current had a very small IA current with fast inac
tivation or only had a IK current with slow activation and inactivation rates (Table 1, Fig. 1 and 5). Type IV IA was only a small size current with fast inactivation rates which blocked by -30 mV pre-pulse. Half-maximum activation and halfmaximum inactivation rates were -26.9 mV and -79.1 mV. IK was relatively a large current and showed the slow inactivation rates.
The IA was only sensitive to 4-AP but IK was significantly blocked by both TEA and 4-AP (Fig. 5)
Discussion
Primary afferent neurons of the mammalian DRG and TRG are classified on basis of the morphological and electro physiological characteristics of neurons. Large neurons with myelinated Aα and β fibers propagating touch and pressure have a fast conducting velocity whereas small neurons with myelinated Aδ and unmyelinated C fibers propagating pain

and temperature have a slow conducting velocity [9]. Rat TRG neuron isolated by enzyme in this study showed various sizes ranging from 15 to 40 µm. However, properties of the neuronal action potential are known to be associated with the cell types at lesser extent; long action potential with inflected repolarization is mainly recorded from Aβ and C neurons and short action potential without plateau during falling phase is recorded from Aα and Aδ [10].
Intracellular recordings in the mammalian TRG neurons have shown that three types of action potential exist; 1) fast spikes, most of which are completely blocked by tetrodotoxin (TTX), 2) CO2+-and TTX-resistant humped spikes [11] and 3) slowly decaying TTX-resistant and Cd2+-sensitive action potentials [12]. These diversities of neuronal size and action potential in TRG may reflect that various types of voltage-dependent ion channels are expressed in TRG. In fact, at least two types of voltage-gated sodium current (INa) distinguished by their sensitivity to TTX [13-15] and T, L, N and P types of voltage-gated calcium current (ICa) have been reported to exist in DRG and TRG. However, diversity and characteristics of voltage-gated potassium currents have been not well studied in sensory neurons because characteristics of voltage gated K+ current are changed according to developmental stage and have complicated properties [16].
Voltage-gated K+ currents are traditionally classified in terms of three families, distinguished mainly by their responses to changes in membrane potential ; 1) transient (Atype) K+ current activated by depolarization and decayed spontaneously and rapidly while the depolarization is maintained, 2) delayed rectifier K+ current with a brief delay following the onset of a membrane depolarization and sustained while the depolarization is maintained and 3) inward rectifier opened by a large hyperpolarization [17]. Transient A type and delayed rectifier K+ current are known to exist in neuronal cell. Even in this experiment, whole K+ currents were composed of a transient and a delayed outward current in TRG neurons but inward rectifier currents were not observed at voltage steps more than -80 mV.
Gold et al. (1996) recently reported that DRG sensory neurons express at least different six voltage-gated K+ currents in electrophysiological and pharmacological properties; three transient and three sustained currents [7]. However, characterization and diversity of voltage-gated K+ current in TRG have been not studied. Therefore, in this study voltage-gated K+ currents in TRG were firstly separated on

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Seung Ho Choi, Chang Youn, Ji-Il Park, Soon-Yeon Jeong, Won-Man Oh, Ji-Yeon Jung, and Won-Jae Kim

basis of total shape of whole current composed of a transient outward current and a delayed sustained outward current unlike a previous study of which each transient and sustained K+ currents were independently separated in DRG neurons. Furthermore, electrophysiological kinetics and pharmacological properties of various voltage-gated K+ current were examined in this study.
In this study, at least four different voltage-gated outward K+ currents were observed in TRG neurons; 1) type I outward K+ current characterized as a whole current composed of a large rapid, transient outward current (IA) with slow inactivation rates and a small delayed, sustained outward current (IK) with fast inactivation rate, 2) type II K+ current characterized as a whole current composed of a large IA with slow inactivation rate and ad medium size IK with slow inactivation rate, 3) type III K+ current composed of a medium size IA with fast inactivation and a large IK with very slow inactivation, and 4) type IV K+ current composed of a very small IA current with inactivation and a large IK with very slow inactivation.
In the present study, four voltage-gate K+ currents found in TRG neurons showed apparent difference in electrokinetic and pharmacological properties. The degree of IA size among four K+ current types in TRG neuron was in order of type I > type II > type III > type IV. IA inactivation rates of type I and II K+ currents were relatively slow or a little slow while those of type III and IV were rapid. IA currents in all K current types were sensitive to 4-AP, a voltage-gated K channel blocker, indicating that 4-AP significantly decreased IA current evoked by voltage clamping in all types. These results were consistent with previous reports that 4- AP is sensitive to the transient A current [2,18]. Even if TEA, a voltage-gated K+ channel blocker, has been known to be more sensitive to IK than IA [19], TEA significantly decreased IA in type I and II K+ currents of TRG. In the present study, type I and II K+ currents were found in large size TRG neurons (>30 µm) while type III and IV K+ currents were observed in small size TRG neuron (<30 µm). These results suggest that type I and II K+ currents may play a role in regulation of spike frequency and resting membrane potential in TRG large neurons with fast conducting velocity, whereas type III and IV K+ currents may play a pivotal role in regulation of those in small neuron with slow conducting velocity.
On the other hand, physiological role for various voltagegated K+ currents in TRG was not clear in this experiment.

However, it was speculated how various K+ currents with respect to somatic sense properties might regulate neuronal excitability. For an example, a slowly inactivating transient K+ current in sensory neurons functions to limit excitability, because a selective block of the current decreases both action potential-threshold and accommodation [5]. These changes are associated with sensitization of nociceptor by hyperalgesic inflammatory agents such as prostaglandin and serotonin, suggesting that these agents might modulate IA currents in nociceptive neurons. In addition, various delayed IK current may be responsible for repolarizing changes of the action potential, resulting into longer action potential and increased neurotransmitter release.
The role of K+ currents in the cell body is less clear, because there is evidence that antidromically conducting action potentials fail to penetrate the cell body [20]. However, there is a growing body of evidence to suggest that the cell body becomes a source of excitability after injury [21-23]. Thus an injury-induced modulation of the K+ currents presented in the cell body could contribute to these changes in excitability.
In summary, at least four different voltage-gated K+ currents in electrophysical and pharmacological properties existed in TRG neurons of the rats.
Acknowledgements
This research was supported by a grant from Chonnam National University Hospital Research Institute of Clinical Medicine and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science and Technology (20100006901 and 2010-0022519). Also, this work was supported the National Research Foundation of Korea (NRF) grants funded by the Korea government (MEST) (2011-0030761 and 2011-0029663).
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CurrentsNeuronsTeaInactivation RateTrg