Martentoxin: A unique ligand of BK channels

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Author:
TAO Jie(Laboratory of Neuropharmacology and Neurotoxicology, Shanghai University, Shanghai 200444, China)
SHI Jian(Laboratory of Neuropharmacology and Neurotoxicology, Shanghai University, Shanghai 200444, China)
LIU Zhi-Rui(Laboratory of Neuropharmacology and Neurotoxicology, Shanghai University, Shanghai 200444, China)
JI Yong-Hua(Laboratory of Neuropharmacology and Neurotoxicology, Shanghai University, Shanghai 200444, China)
Journal Title:
Acta Physiologica Sinica
Issue:
Volume 64, Issue 04, 2012
DOI:
Key Word:
BK channels; martentoxin; Ca2+ sensitivity; β subunit; toxin-channel interaction

Abstract: The large-conductance calcium-activated potassium (BK) channels distributed in both excitable and non-excitable cells are key participants in a variety of physiological functions.By employing numerous high-affinity natural toxins originated from scorpion venoms the pharmacological and structural characteristics of these channels tend to be approached A 37-residue short-chain peptide,named as martentoxin,arising from the venom of the East-Asian scorpion (Buthus martensi Karsch) has been investigated with a comparatively higher preference for BK channels over other voltage-gated potassium (Kv) channels.Up to now,since the specific drug tool probing for clarifying structure-function of BK channel subtypes and related pathology remain scarce,it is of importance to illuminate the underlying mechanism of molecular interaction between martentoxin and BK channels.As for it,the current review will address the recent progress on the studies of pharmacological characterizations and molecular determinants of martentoxin targeting on BK channels.

  • 1.McManus OB.Calcium-activated potassium channels:regulation by calcium.J Bioenerg Biomembr 1991; 23(4):537-560.
  • 2.Pallotta BS.N-bromoacetamide removes a calcium-dependent component of channel opening from calcium-activated potassium channels in rat skeletal muscle.J Gen Physiol 1985; 86(5):601-611.
  • 3.Nelson MT,Quayle JM.Physiological roles and properties of potassium channels in arterial smooth muscle.Am J Physiol 1995; 268(4 Pt 1):C799-C822.
  • 4.Hurley BR,Preiksaitis HG,Sims SM.Characterization and regulation of Ca2+-dependent K+ channels in human esophageal smooth muscle.Am J Physiol 1999; 276(4 Pt 1):G843-G852.
  • 5.Petkov GV,Boney AD,Heppner TJ,Brenner R,Aldrich RW,Nelson MT.Betal-subunit of the Ca2+-activated K+ channel regulates contractile activity of mouse urinary bladder smooth muscle.J Physiol 2001; 537(Pt 2):443-452.
  • 6.Nelson MT,Bonev AD.The betal subunit of the Ca2+-sensitive K+ channel protects against hypertension.J Clin Invest 2004; 113(7):955-957.
  • 7.Navarro-Antolin J,Levitsky KL,Calderon E,Ordoncz A,Lopez-Barneo J.Decreased expression of maxi-K+ channel betal-subunit and altered vasoregulation in hypoxia.Circulation 2005; 112(9):1309-1315.
  • 8.Robitaille R,Charlton MP.Presynaptic calcium signals and transmitter release are modulated by calcium-activated potassium channels.J Neurosci 1992; 12(1):297-305.
  • 9.Poolos NP,Johnston D.Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CAI pyramidal neurons.J Neurosci 1999; 19(13):5205-5212.
  • 10.MacDermott AB,Weight FF.Action potential repolarization may involve a transient,Ca2+-sensitive outward current in a vertebrate neurone.Nature 1982; 300(5888):185-188.
  • 11.Jin W,Sugaya A,Tsuda T,Ohguchi H,Sugaya E.Relationship between large conductance calcium-activated potassium channel and bursting activity.Brain Res 2000; 860(1-2):21-28.
  • 12.Golding NL,Jung HY,Mickus T,Spruston N.Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CAI pyramidal neurons.J Neurosci 1999; 19(20):8789-8798.
  • 13.Du W,Bautista JF,Yang H,Diez-Sampedro A,You SA,Wang L,Kotagal P,Luders HO,Shi J,Cui J,Richerson GB,Wang QK.Calcium-sensitive potassium channelopathy in human epilepsy and paroxysmal movement disorder.Nat Genet 2005; 37(7):733-738.
  • 14.Marty A.The physiological role of calcium-dependent channels.Trends Neurosci 1989; 12(11):420-424.
  • 15.Lingle CJ,Solaro CR,Prakriya M,Ding JP.Calcium-activated potassium channels in adrenal chromaffin cells.Ion Channels 1996; 4:261-301.
  • 16.Wiecha J,Munz B,Wu Y,Noll T,Tillmanns H,Waldecker B.Blockade of Ca2+-activated K+ channels inhibits proliferation of human endothelial cells induced by basic fibroblast growth factor.J Vasc Res 1998; 35(5):363-371.
  • 17.Weaver AK,Liu X,Sontheimer H.Role for calcium-activated potassium channels (BK) in growth control of human malignant glioma cells.J Neurosci Res 2004; 78(2):224-234.
  • 18.Kraft R,Krause P,Jung S,Basrai D,Liebmann L,Bolz J,Patt S.BK channel openers inhibit migration of human glioma cells.Pflugers Arch 2003; 446(2):248-255.
  • 19.Shen KZ,Lagrutta A,Davies NW,Standen NB,Adelman JP,North RA.Tetraethylammonium block of Slowpoke calcium-activated potassium channels expressed in Xenopus oocytes:evidence for tetrameric channel formation.Pflugers Arch 1994; 426(5):440-445.
  • 20.Atkinson NS,Robertson GA,Ganetzky B.A component of calcium-activated potassium channels encoded by the Drosophila slo locus.Science 1991; 253(5019):551-555.
  • 21.Wallner M,Meera P,Toro L.Determinant for beta-subunit regulation in high-conductance voltage-activated and Ca2+-sensitive K+ channels:an additional transmembrane region at the N terminus.Proc Natl Acad Sci U S A 1996; 93(25):14922-14927.
  • 22.Schreiber M,Salkoff L.A novel calcium-sensing domain in the BK channel.Biophys J 1997; 73(3):1355-1363.
  • 23.Orio P,Rojas P,Ferreira G,Latorre R.New disguises for an old channel:MaxiK channel beta-subunits.News Physiol Sci 2002; 17:156-161.
  • 24.Shipston MJ.Alternative splicing of potassium channels:a dynamic switch of cellular excitability.Trends Cell Biol 2001; 11(9):353-358.
  • 25.Lippiat JD,Standen NB,Harrow ID,Phillips SC,Davies NW.Properties of BK(Ca) channels formed by bicistronic expression of hSloalpha and beta 1-4 subunits in HEK293 cells.J Membr Biol 2003; 192(2):141-148.
  • 26.Meera P,Wallner M,Toro L.A neuronal beta subunit (KCN-MB4) makes the large conductance,voltage-and Ca2+-activated K+ channel resistant to charybdotoxin and iberiotoxin.Proc Natl Acad Sci U S A 2000; 97(10):5562-5567.
  • 27.Dworetzky SI,Boissard CG,Lum-Ragan JT,McKay MC,Post-Munson DJ,Trojnacki JT,Chang CP,Gribkoff VK.Phenotypic alteration of a human BK (hSlo) channel by hSlobeta subunit coexpression:changes in blocker sensitivity.activation/relaxation and inactivation kinetics,and protein kinase A modulation.J Neurosci 1996; 16(15):4543-4550.
  • 28.McManus OB,Helms LM,Pallanck L,Ganetzky B,Swanson R,Leonard RJ.Functional role of the beta subunit of high conductance calcium-activated potassium channels.Neuron 1995; 14(3):645-650.
  • 29.Meera P,Wallner M,Jiang Z,Toro L.A calcium switch for the functional coupling between alpha (hslo) and beta subunits (KV,Ca beta) of maxi K channels.FEBS Lett 1996;382(1-2):84-88.
  • 30.Brenner R,Jegla TJ,Wickenden A,Liu Y,Aldrich RW.Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits,hKCNMB3 and hKCNMB4.J Biol Chem 2000; 275(9):6453-6461.
  • 31.Liu ZR,Ye P,Ji YH.Exploring the obscure profiles of pharmacological binding sites on voltage-gated sodium channels by BmK neurotoxins.Protein Cell 2011; 2(6):437-444.
  • 32.Ji YH,Liu T.The study of sodium channels involved in pain responses using specific modulators.Acta Physiol Sin (生理学报) 2008; 60(5):628-634.
  • 33.Zhu MM,Tao J,Tan M,Yang HT,Ji YH.U-shaped dose-dependent effects of BmK AS,a unique scorpion polypeptide toxin,on voltage-gated sodium channels.Br J Pharmacol 2009; 158(8):1895-1903.
  • 34.Romi-Lebrun R,Martin-Eauclaire MF,Escoubas P,Wu FQ,Lebrun B,Hisada M,Nakajima T.Characterization of four toxins from Buthus martensi scorpion venom,which act on apamin-sensitive Ca2+-activated K-channels.Eur J Biochem 1997; 245(2):457-464.
  • 35.Tong QC,Zhang Y,Li DP,Zhou ZN,Ji YH.The blocking effect of BmP02,one novel short-chain scorpion peptide on transient outward K+ channel of adult rat ventricular myocyte.Regul Pept 2000; 90(1-3):85-92.
  • 36.Xu Y,Wu J,Pei J,Shi Y,Ji Y,Tong Q.Solution structure of BmP02,a new potassium channel blocker from the venom of the Chinese scorpion Buthus martensi Karsch.Biochemistry 2000; 39(45):13669-13675.
  • 37.Vacher H,Romi-Lebrun R,Mourre C,Lebrun B,Kourrich S,Masmejean F,Nakajima T,Legros C,Crest M,Bougis PE,Martin-Eauclaire MF.A new class of scorpion toxin binding sites related to an A-type K+ channel:pharmacological characterization and localization in rat brain.FEBS Lett 2001;501(1):31-36.
  • 38.Yao J,Chen X,Li H,Zhou Y,Yao L,Wu G,Zhang N,Zhou Z,Xu T,Wu H,Ding J.BmP09,a "long chain" scorpion peptide blocker of BK channels.J Biol Chem 2005; 280(15):14819-14828.
  • 39.Ji YH,Wang WX,Ye JG,He LL,Li YJ,Yan YP,Zhou Z.Martentoxin,a novel K+-channel-blocking peptide:purification,cDNA and genomic cloning,and electrophysiological and pharmacological characterization.J Neurochem 2003;84(2):325-335.
  • 40.Marshall DL,Vatanpour H,Harvey AL,Boyot P,Pinkasfeld S,Doljansky Y,Bouet F,Menez A.Neuromuscular effects of some potassium channel blocking toxins from the venom of the scorpion Leiurus quinquestriatus hebreus.Toxicon 1994;32(11):1433-1443.
  • 41.Escoubas P,Celerier ML,Nakajima T.High-performance liquid chromatography matrix-assisted laser desorption/ionization time-of-flight mass spectrometry peptide fingerprinting of tarantula venoms in the genus Brachypelma:chemotaxonomic and biochemical applications.Rapid Commun Mass Spectrom 1997; 11(17):1891-1899.
  • 42.Wang YH,Cao ZY,He WY,Yan XZ,Liu X,Liu HY,Liang XT,Yu DQ.1H-NMR signal assignments and secondary structure analysis of martentoxin.J Asian Nat Prod Res 2006; 8(6):511-518.
  • 43.Wang Y,Chen X,Zhang N,Wu G,Wu H.The solution structure of BmTx3B,a member of the scorpion toxin subfamily alpha-KTx16.Proteins 2005; 58(2):489-497.
  • 44.Knaus HG,Folander K,Garcia-Calvo M,Garcia ML,Kaczorowski GJ,Smith M,Swanson R.Primary sequence and immunological characterization of beta-subunit of high conductance Ca2+-activated K-channel from smooth muscle.J Biol Chem 1994; 269(25):17274-17278.
  • 45.Knaus HG,McManus OB,Lee SH,Schmalhofer WA,Garcia-Calvo M,Helms LM,Sanchez M,Giangiacomo K,Reuben JP,Smith AB 3rd,Kaczorowski GJ,Garcia ML.Tremorgenic indole alkaloids potently inhibit smooth muscle highconductance calcium-activated potassium channels.Biochemistry 1994; 33(19):5819-5828.
  • 46.Wallner M,Meera P,Toro L.Molecular basis of fast inactivation in voltage and Ca2+-activated K+ channels:a transmembrane beta-subunit homolog.Proc Natl Acad Sci U S A 1999; 96(7):4137-4142.
  • 47.Liu X,Chang Y,Reinhart PH,Sontheimer H.Cloning and characterization of glioma BK,a novel BK channel isoform highly expressed in human glioma cells.J Neurosci 2002;22(5):1840-1849.
  • 48.Cao ZY,Shen WQ,Pan YP,Xiao X,Liu XM,Wang XL,Liang XT,Yu DQ.Purification,characterization of two peptides from Buthus martensi Karch.J Pept Res 2003; 62(6):252-259.
  • 49.Shi J,He HQ,Zhao R,Duan YH,Chen J,Chen Y,Yang J,Zhang JW,Shu XQ,Zheng P,Ji YH.Inhibition of martentoxin on neuronal BK channel subtype (alpha+beta4):implications for a novel interaction model.Biophys J 2008; 94(9):3706-3713.
  • 50.Tao J,Shi J,Yan L,Chen Y,Duan YH,Ye P,Feng Q,Zhang JW,Shu XQ,Ji YH.Enhancement effects of martentoxin on glioma BK channel and BK channel (alpha+beta1) subtypes.PLoS One 2011; 6(3):e15896.
  • 51.Ransom CB,Liu X,Sontheimer H.BK channels in human glioma cells have enhanced calciun sensitivity.Glia 2002;38(4):281-291.
  • 52.Weaver AK,Bomben VC,Sontheimer H.Expression and function of calcium-activated potassium channels in human glioma cells.Glia 2006; 54(3):223-233.
  • 53.Giangiacomo KM,Garcia ML,McManus OB.Mechanism of iberiotoxin block of the large-conductance calcium-activated potassium channel from bovine aortic smooth muscle.Biochemistry 1992; 31(29):6719-6727.
  • 54.Garcia-Valdes J,Zamudio FZ,Toro L,Possani LD.Slotoxin,alphaKTx1.11,a new scorpion peptide blocker of MaxiK channels that differentiates between alpha and alpha+beta (betal or beta4)complexes.FEBS Lett 2001; 505(3):369-373.
  • 55.Swartz KJ,MacKinnon R.Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites.Neuron 1997; 18(4):665-673.
  • 56.Swartz KJ,MacKinnon R.Mapping the receptor site for hanatoxin,a gating modifier of voltage-dependent K+ channels.Neuron 1997; 18(4):675-682.
  • 57.Ruta V,MacKinnon R.Localization of the voltage-sensor toxin receptor on KvAP.Biochemistry 2004; 43(31):10071-10079.
  • 58.Schmidt D,MacKinnon R.Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane.Proc Natl Acad Sci U S A 2008; 105(49):19276-19281.
  • 59.Knaus HG,Eberhart A,Glossmann H,Munujos P,Kaczorowski GJ,Garcia ML.Pharmacology and structure of high conductance calcium-activated potassium channels.Cell Signal 1994; 6(8):861-870.
  • 60.Jin P,Weiger TM,Levitan IB.Reciprocal modulation between the alpha and beta 4 subunits of hSlo calcium-dependent potassium channels.J Biol Chem 2002; 277(46):43724-43729.
  • 61.Hagen BM,Sanders KM.Deglycosylation of the beta1-subunit of the BK channel changes its biophysical properties.Am J Physiol Cell Physiol 2006; 291(4):C750-C756.
  • 62.Faber ES,Sah P,Ca2+-activated K+ (BK) channel inactivation contributes to spike broadening during repetitive firing in the rat lateral amygdala.J Physiol 2003; 552(Pt 2):483-497.
  • 63.Brenner R,Chen QH,Vilaythong A,Toney GM,Noebcls JL,Aldrich RW.BK channel beta4 subunit reduces dentate gyrus excitability and protects against temporal lobe seizures.Nat Neurosci 2005; 8(12):1752-1759.
  • 64.Gu N,Vervaeke K,Storm JF.BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells.J Physiol 2007; 580(Pt.3):859-882.
  • 65.Yoshida J,Mizuno M,Fujii M,Kajita Y,Nakahara N,Hatano M,Saito R,Nobayashi M,Wakabayashi T,Human gene therapy for malignant gliomas (glioblastoma multiforme and anaplastic astrocytoma) by in vivo transduction with human interferon beta gene using cationic liposomes.Hum Gene Ther 2004; 15(1):77-86.
  • 66.Bontems F,Gilquin B,Roumestand C,Menez A,Toma F.Analysis of side-chain organization on a refined model of charybdotoxin:structural and functional implications.Biochemistry 1992; 31(34):7756-7764.
  • 67.Blanc E,Romi-Lebrun R,Bornet O,Nakajima T,Darbon H.Solution structure of two new toxins from the venom of the Chinese scorpion Buthus martensi Karsch blockers of potassium channels.Biochemistry 1998;37(36):12412-12418.
  • 68.Renisio JG,Lu Z,Blanc E,Jin W,Lewis JH,Bomet O,Darbon H.Solution structure of potassium channel-inhibiting scorpion toxin Lq2.Proteins 1999; 34(4):417-426.
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