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Article in Press ARTICLE IN PRESS Toxicon 50 (2007) 507–517 www.elsevier.com/locate/toxicon Characterization of the excitatory mechanism induced by Jingzhaotoxin-I inhibiting sodium channel inactivation Yucheng Xiao, Jiang Li, Meichun Deng, Changliang Dai, Songping Liangà Life Sciences College, Hunan Normal University, Changsha, Hunan 410081, PR China Received 11 February 2007; received in revised form 15 April 2007; accepted 23 April 2007 Available online 3 May 2007 Abstract We have recently isolated a peptide neurotoxin, Jingzhaotoxin-I (JZTX-I), from Chinese tarantula Chilobrachys jingzhao venom that preferentially inhibits cardiac sodium channel inactivation and may define a new subclass of spider sodium channel toxins. In this study, we found that in contrast to other spider sodium channel toxins acting presynaptically rather than postsynaptically, JZTX-I augmented frog end-plate potential amplitudes and caused an increase in both nerve mediated and unmediated muscle twitches. Although JZTX-I does not negatively shift sodium channel activation threshold, an evident increase in muscle fasciculation was detected. In adult rat dorsal root ganglion neurons JZTX-I (1 mM) induced a significant sustained tetrodotoxin-sensitive (TTX-S) current that did not decay completely during 500 ms and was inhibited by 0.1 mM TTX or depolarization due to voltage-dependent acceleration of toxin dissociation. Moreover, JZTX-I decreased closed-state inactivation and increased the rate of recovery of sodium channels, which led to an augmentation in TTX-S ramp currents and decreasing the amount of inactivation in a use-dependant manner. Together, these data suggest that JZTX-I acted both presynaptically and postsynaptically and facilitated the neurotransmitter release by biasing the activities of sodium channels towards open state. These actions are similar to those of scorpion a-toxin Lqh II. r 2007 Elsevier Ltd. All rights reserved. Keywords: Sodium channels; Spider toxin; Dorsal root ganglia; Whole-cell recording 1. Introduction tissues. Their characteristic structures are found to contain a pore-forming functional a subunit and The opening of voltage-gated sodium channels several auxiliary b subunits (b1–b4). The two kinds (VGSCs) plays a critical role in the generation and of subunit interact with each other by covalent or propagation of action potentials on excitable non-covalent bonds (Ogata and Tatebayashi, 1993; Catterall, 2000; Yu et al., 2003). Although up to 10 Abbreviations: dTc, d-Tubocurarine; DRG, dorsal root gang- mammalian VGSC isoforms (Nav1.1–1.9 and Navx) lia; ICK, inhibitor cystein knot; JZTX, Jingzhaotoxin; TTX, have been identified, cloned and functionally tetrodotoxin; TTX-R, tetrodoxin resistant; TTX-S, tetrodotoxin characterized (Ogata and Ohishi, 2002), they are sensitive; VGSC (and Nav), voltage-gated sodium channel ÃCorresponding author. Tel.: +86 731 8872556; highly conserved during evolution based on the fax: +86 731 8861304. analysis of a subunit protein sequences and main- E-mail address: [email protected] (S. Liang). taining similar pharmacological functions (Catterall 0041-0101/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.toxicon.2007.04.018 ARTICLE IN PRESS 508 Y. Xiao et al. / Toxicon 50 (2007) 507–517 et al., 2003). Some VGSC isoforms may be unrelated to toxin partitioning in the phospholipid expressed selectively in certain tissues and even the bilayer of neuronal membranes (Cohen et al., 2006; same isoform can display quantitative differences in Lee and MacKinnon, 2004). channel kinetics after expression in different tissues. Jingzhaotoxin-I (JZTX-I) is a VGSC toxin newly Cummins et al. (2001) demonstrated that the reported from Chinese tarantula Chilobrachys jingz- repriming kinetics for rat Nav1.3 were twofold hao venom (Zhu et al., 2001). Composed of 33 faster in neurons than in human embryonic kidney residues and stabilized by three disulfide bonds 293 cells. Furthermore, mutants of VGSC a subunit (I–IV, II–V, III–VI), the neurotoxin preferentially proteins can occur naturally, leading to dysfunction inhibits cardiac sodium channel inactivation (Xiao of sodium channels. For example, I848T and L858H et al., 2005). The characteristics of its secondary mutants of human Nav1.7 cause a significant structure are similar to that of huwentoxin-I in hyperpolarizing shift in the V1/2 of channel activa- solution, which mainly contains a short triple- tion (Cummins et al., 2004). To date, over 150 stranded antiparallel b-sheet (Liang et al., 2000; naturally occurring VGSC mutants have been Zeng et al., 2005). More recently, we reported that characterized in several human hereditary diseases, the toxin also inhibited Kv2.1 and Kv4.1, but the such as skeletal muscle myotonias, episodic ataxia affinities were over fivefold lower than to neuronal and epilepsy (Meisler and Kearney, 2005). There- TTX-S VGSCs (Yuan et al., 2007). In this study, we fore, novel potent VGSC ligands will be of great characterized the excitatory responses of JZTX-I on significance as drugs for alleviating diseases and as several in vitro preparations and the underlying tools for investigating the structure and function mechanism on TTX-S VGSCs expressed in adult rat relationships of sodium channels. dorsal root ganglion (DRG) neurons. For defense or predation, many animals evolve a venom gland to secrete toxins targeting sodium 2. Methods channel. Most of them are of protein structures stabilized by three or four intramolecular disulfide 2.1. Toxin purification bridges. They can be folded into inhibitor cystein knot (ICK) or a/b motifs, the former being frequent JZTX-I was fractionated from Chinese tarantula in spider toxins, sea anemone toxins and conotoxins C. jingzhao venom, using ion-exchange chromato- and the latter in scorpion toxins (Xiao et al., 2004; graphy followed by reverse-phase high pressure Karbat et al., 2004). These VGSC modulating liquid chromatography as previously described toxins have been classified into two groups accord- (Xiao et al., 2005). After the purity of the sample ing to the properties: (1), pore-blocking toxins, such was up to 99% calculated by the analysis of matrix- as m-conotoxins, which occlude the channel pore to assisted laser desorption/ionization time-of-flight block inward sodium currents by binding to site 1 in mass spectrometry and eluted peak area, it was a manner similar to tetrodotoxin (TTX) and stored at À20 1C until required. saxitoxin (Shon et al., 1998). Unaffecting sodium channel activation and inactivation kinetics, several tarantula toxins, such as huwentoxin-IV, hainan- 2.2. Tissue preparation toxin-III and hainantoxin-IV, are also assumed to belong to the family (Peng et al., 2002; Xiao and Phrenic nerve-diaphragm preparation was acutely Liang, 2003); (2), gate-modifying toxins, such as isolated from the 20 g Kunming mouse of either sex a/b-scorpion toxins and sea anemone toxins, which as described by Zhou et al. (1997). After isolation, modulate the movement of the voltage sensor to the fresh preparations were immediately immersed affect the activities of activation gate and inactiva- into Tyrode’s solution containing (mM): NaCl tion ball by binding to neuronal site 2–6 (Rogers 143.0, KCl 5.4, NaH2PO4 0.3, MgCl2 0.5, glucose et al., 1996; Richard Benzinger et al., 1999). 10.0, HEPES 5.0, CaCl2 1.8 at pH7.2. Tyrode’s b-Scorpion toxins binding to neuronal site 4 toxins solution was kept to be bubbled at 30–32 1C by 95% trap the voltage sensor in the activated state in a O2 and 5% CO2. Electrical stimulation was applied voltage dependent but concentration-independent indirectly to the phrenic nerve with a suction manner (Cestele et al., 2006). Different from electrode, or directly to the muscle using a same potassium channel modifiers, the underpinning protocol at a frequency of 0.06 Hz (supramaximal, mechanism of this is clearly disclosed to be 0.2 s, square wave). ARTICLE IN PRESS Y. Xiao et al. / Toxicon 50 (2007) 507–517 509 Vas deferens preparation was acutely dissociated The output electrical signals after amplification from male Sprague–Dawley rats with about 200 g were displayed and simultaneously recorded using and bisected to be prostatic and epididymal a BL-420 biology function laboratory system segments as described by Liang et al. (2000). Before (Chengdu instrument, China). All sciatic nerve– both segments of the vas deferens with length of satorius muscle preparations were immersed in 2 cm were immerged into 5 ml physiological saline Ringer solution containing 5 mM d-tubocurarine solutions bubbled by 95% O2 and 5% CO2 and (dTc) for 10 min, and then the innervated muscle maintained at 33 1C, the top of each tissue was fiber at end-plate area was impaled with a micro- attached to an electromechanical transducer and the electrode. Suprathreshold electrical stimulation bottom attached to a movable support. The tissue (3 V, 1 ms) was continuously applied on the sciatic was straddled with platinum stimulating electrodes. nerve at a constant frequency of 1 Hz for 1 min. For For prostatic segments, the solution contained control and toxin tested groups, the preparations (mM): NaCl 119.0, KCl 4.7, CaCl2 2.5, NaHCO3 were treated under the same processes. 2.5, MgSO4?7H2O 1.2, KH2PO4 1.2, Glucose 11.0, EDTA 0.026 at pH 7.3, in which EDTA was used to 2.4. Patch-clamp recordings in rat DRG neurons eliminate the fasciculation, while for epididymal segments the solution contained (mM): NaCl 118.4; Rat DRG neurons were acutely dissociated and KCl 4.7; MgSO4 1.2; KH2PO4 1.2; CaCl2 2.5; maintained in a short-term primary culture accord- NaHCO3 25; D-glucose 11.1, as provided by Rash ing to the procedures adapted from (Xiao et al. et al. (2000). The prostatic segment of the vas deferens (2005). Sodium currents were recorded from ex- was stimulated with single electrical field pulses perimental cells using an EPC9 patch clamp (100 V, 0.1 ms wave width) for every 5 s while no amplifier (HEKA, Germany) at room temperature electrical stimulation was applied on the epididymal (22–25 1C).
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