Targeting voltage sensors in sodium channels with spider toxins

Trends in Pharmacological Sciences

Volumn 31, Issue 4, 2010, Pages 175-182

  Bosmans, Frank ^a,b   Swartz, Kenton J ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

HANATOXIN; LIPID; PROTOXIN 1; PROTOXIN 2; SPIDER VENOM; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

CHANNEL GATING; CHEMICAL STRUCTURE; ELECTRICITY; HYDROPHOBICITY; LIPID MEMBRANE; MOLECULAR INTERACTION; MUTAGENESIS; MUTATION; NERVE CONDUCTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SENSOR;

AMINO ACID SEQUENCE; ANIMALS; DRUG DELIVERY SYSTEMS; HUMANS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SPIDER VENOMS;

EID: 77950515381     PISSN: 01656147     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tips.2009.12.007     Document Type: Review

References (87)

1. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 2000, 26:13-25.
2. Hille B. Ion channels of excitable membranes 2001, Sinauer Associates, Incorporated.
3. Cannon S.C. Pathomechanisms in channelopathies of skeletal muscle and brain. Annu. Rev. Neurosci. 2006, 29:387-415.
4. George A.L. Inherited disorders of voltage-gated sodium channels. J. Clin. Invest. 2005, 115:1990-1999.
5. Goldin A.L. Resurgence of sodium channel research. Annu. Rev. Physiol. 2001, 63:871-894.
6. Waxman S.G., Dib-Hajj S. Erythermalgia: molecular basis for an inherited pain syndrome. Trends Mol. Med. 2005, 11:555-562.
7. Cox J., et al. An SCN9A channelopathy causes congenital inability to experience pain. Nature 2006, 444:894-898.
8. Catterall W.A., et al. International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 2005, 57:397-409.
9. Chanda B., Bezanilla F. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. J. Gen. Physiol. 2002, 120:629-645.
10. Horn R., et al. Immobilizing the moving parts of voltage-gated ion channels. J. Gen. Physiol. 2000, 116:461-476.
11. Sheets M.F., et al. The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys. J. 1999, 77:747-757.
12. Bosmans F., et al. Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 2008, 456:202-208.
13. Mebs D. Venomous and Poisonous Animals: A Handbook for Biologists, Toxicologists and Toxinologists, Physicians and Pharmacists 2002, Medpharm.
14. Catterall W.A., et al. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49:124-141.
15. Terlau H., Olivera B.M. Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol. Rev. 2004, 84:41-68.
16. Honma T., Shiomi K. Peptide toxins in sea anemones: structural and functional aspects. Mar. Biotechnol. (NY) 2006, 8:1-10.
17. Rodriguez de la Vega R.C., Possani L.D. Overview of scorpion toxins specific for Na+ channels and related peptides: biodiversity, structure-function relationships and evolution. Toxicon 2005, 46:831-844.
18. Escoubas P., et al. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol. Pharmacol. 2002, 62:48-57.
19. + channel. Nature 2003, 422:180-185.
20. Swartz K.J. Tarantula toxins interacting with voltage sensors in potassium channels. Toxicon 2007, 49:213-230.
21. Alabi A.A., et al. Portability of paddle motif function and pharmacology in voltage sensors. Nature 2007, 450:370-375.
22. Swartz K.J., MacKinnon R. Mapping the receptor site for hanatoxin, a gating modifier of voltage-dependent K+ channels. Neuron 1997, 18:675-682.
23. Swartz K.J., MacKinnon R. Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites. Neuron 1997, 18:665-673.
24. Phillips L.R., et al. Voltage-sensor activation with a tarantula toxin as cargo. Nature 2005, 436:857-860.
25. +) channel. J. Gen. Physiol. 2000, 115:673-684.
26. Ruta V., MacKinnon R. Localization of the voltage-sensor toxin receptor on KvAP. Biochemistry 2004, 43:10071-10079.
27. Lee H.C., et al. Interaction between extracellular Hanatoxin and the resting conformation of the voltage-sensor paddle in Kv channels. Neuron 2003, 40:527-536.
28. Bezanilla F., Stefani E. Gating currents. Methods Enzymol. 1998, 293:331-352.
29. Middleton R.E., et al. Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 2002, 41:14734-14747.
30. Edgerton G.B., et al. Evidence for multiple effects of ProTxII on activation gating in Na(V)1.5. Toxicon 2008, 52:489-500.
31. Schmalhofer W.A., et al. ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol. Pharmacol. 2008, 74:1476-1484.
32. Smith J.J., et al. Differential phospholipid binding by site 3 and site 4 toxins. Implications for structural variability between voltage-sensitive sodium channel domains. J. Biol. Chem. 2005, 280:11127-11133.
33. Smith J.J., et al. Molecular interactions of the gating modifier toxin ProTx-II with NaV 1.5: implied existence of a novel toxin binding site coupled to activation. J. Biol. Chem. 2007, 282:12687-12697.
34. Sokolov S., et al. Inhibition of sodium channel gating by trapping the domain II voltage sensor with protoxin II. Mol. Pharmacol. 2008, 73:1020-1028.
35. Wang M., et al. JZTX-IV, a unique acidic sodium channel toxin isolated from the spider Chilobrachys jingzhao. Toxicon 2008, 52:871-880.
36. Corzo G., et al. Solution structure and alanine scan of a spider toxin that affects the activation of mammalian voltage-gated sodium channels. J. Biol. Chem. 2007, 282:4643-4652.
37. Escoubas P., Rash L. Tarantulas: eight-legged pharmacists and combinatorial chemists. Toxicon 2004, 43:555-574.
38. Wang J.M., et al. Molecular surface of tarantula toxins interacting with voltage sensors in K(v) channels. J. Gen. Physiol. 2004, 123:455-467.
39. +) channels: common surface features of gating modifier toxins. J. Mol. Biol. 2000, 297:771-780.
40. Bosmans F., et al. Four novel tarantula toxins as selective modulators of voltage-gated sodium channel subtypes. Mol. Pharmacol. 2006, 69:419-429.
41. Xiao Y., et al. Synthesis and characterization of huwentoxin-IV, a neurotoxin inhibiting central neuronal sodium channels. Toxicon 2008, 51:230-239.
42. Jung H.J., et al. Solution structure and lipid membrane partitioning of VSTx1, an inhibitor of the KvAP potassium channel. Biochemistry 2005, 44:6015-6023.
43. Diochot S., et al. Effects of phrixotoxins on the Kv4 family of potassium channels and implications for the role of Ito1 in cardiac electrogenesis. Br. J. Pharmacol. 1999, 126:251-263.
44. Sanguinetti M.C., et al. Heteropodatoxins: peptides isolated from spider venom that block Kv4.2 potassium channels. Mol. Pharmacol. 1997, 51:491-498.
45. Cestele S., et al. Voltage sensor-trapping: enhanced activation of sodium channels by beta-scorpion toxin bound to the S3-S4 loop in domain II. Neuron 1998, 21:919-931.
46. Cohen L., et al. Common features in the functional surface of scorpion beta-toxins and elements that confer specificity for insect and mammalian voltage-gated sodium channels. J. Biol. Chem. 2005, 280:5045-5053.
47. Cahalan M.D. Modification of sodium channel gating in frog myelinated nerve fibres by Centruroides sculpturatus scorpion venom. J. Physiol. 1975, 244:511-534.
48. Koppenhofer E., Schmidt H. [Effect of scorpion venom on ionic currents of the node of Ranvier. II. Incomplete sodium inactivation]. Pflugers Arch. 1968, 303:150-161.
49. Koppenhofer E., Schmidt H. [Effect of scorpion venom on ionic currents of the node of Ranvier. I. The permeabilities PNa and PK]. Pflugers Arch. 1968, 303:133-149.
50. + channel alpha subunit. J. Biol. Chem. 1996, 271:15950-15962.
51. Rochat H., et al. Interaction of scorpion toxins with the sodium channel. J. Physiol. (Paris) 1984, 79:334-337.
52. Campos F.V., et al. Alpha-scorpion toxin impairs a conformational change that leads to fast inactivation of muscle sodium channels. J. Gen. Physiol. 2008, 132:251-263.
53. Campos F.V., et al. beta-Scorpion toxin modifies gating transitions in all four voltage sensors of the sodium channel. J. Gen. Physiol. 2007, 130:257-268.
54. Chakrapani S., et al. Structural dynamics of an isolated voltage-sensor domain in a lipid bilayer. Structure 2008, 16:398-409.
55. + channel. Nature 2003, 423:33-41.
56. + channel. Nature 2003, 423:42-48.
57. + channel in a lipid membrane-like environment. Nature 2007, 450:376-382.
58. + channel. Cell 2005, 123:463-475.
59. Swartz K.J. Sensing voltage across lipid membranes. Nature 2008, 456:891-897.
60. Xiao Y., et al. Tarantula huwentoxin-IV inhibits neuronal sodium channels by binding to receptor site 4 and trapping the domain II voltage sensor in the closed configuration. J. Biol. Chem. 2008, 283:27300-27313.
61. Corzo G., et al. Distinct primary structures of the major peptide toxins from the venom of the spider Macrothele gigas that bind to sites 3 and 4 in the sodium channel. FEBS Lett. 2003, 547:43-50.
62. Ramu Y., et al. Enzymatic activation of voltage-gated potassium channels. Nature 2006, 442:696-699.
63. Schmidt D., et al. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 2006, 444:775-779.
64. + channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19276-19281.
65. + channels. Nature 2008, 451:826-829.
66. Lee S.Y., MacKinnon R. A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom. Nature 2004, 430:232-235.
67. Milescu M., et al. Tarantula toxins interact with voltage sensors within lipid membranes. J. Gen. Physiol. 2007, 130:497-511.
68. Milescu M., et al. Interactions between lipids and voltage sensor paddles detected with tarantula toxins. Nat. Struct. Mol. Biol. 2009, 16:1080-1085.
69. Swartz K.J., MacKinnon R. An inhibitor of the Kv2.1 potassium channel isolated from the venom of a Chilean tarantula. Neuron 1995, 15:941-949.
70. + channels. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8585-8589.
71. Edgerton G.B., et al. Modification of gating kinetics in Cav3.1 by the tarantula toxin ProTxII. Biophys. J. 2007, 601a-1601a.
72. Lee C.W., et al. Solution structure and functional characterization of SGTx1, a modifier of Kv2.1 channel gating. Biochemistry 2004, 43:890-897.
73. Suchyna T.M., et al. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J. Gen. Physiol. 2000, 115:583-598.
74. Siemens J., et al. Spider toxins activate the capsaicin receptor to produce inflammatory pain. Nature 2006, 444:208-212.
75. Momin A., Wood J.N. Sensory neuron voltage-gated sodium channels as analgesic drug targets. Curr. Opin. Neurobiol. 2008, 18:383-388.
76. Ashcroft F. Ion channels and disease 1999, Elsevier.
77. Bosmans F., et al. Animal Toxins: State of the Art 2009, Editora UFMG.
78. Xiao Y., et al. Jingzhaotoxin-I, a novel spider neurotoxin preferentially inhibiting cardiac sodium channel inactivation. J. Biol. Chem. 2005, 280:12069-12076.
79. Liao Z., et al. Solution structure of Jingzhaotoxin-III, a peptide toxin inhibiting both Nav1.5 and Kv2.1 channels. Toxicon 2007, 50:135-143.
80. Bennett P.B., et al. Molecular mechanism for an inherited cardiac arrhythmia. Nature 1995, 376:683-685.
81. Spampanato J., et al. Generalized epilepsy with febrile seizures plus type 2 mutation W1204R alters voltage-dependent gating of Na(v)1.1 sodium channels. Neuroscience 2003, 116:37-48.
82. Bulaj G. Integrating the discovery pipeline for novel compounds targeting ion channels. Curr. Opin. Chem. Biol. 2008, 12:441-447.
83. Craik D.J., Adams D.J. Chemical modification of conotoxins to improve stability and activity. ACS Chem. Biol. 2007, 2:457-468.
84. + channel. Neuron 1996, 16:1169-1177.
85. Ahern C.A., Horn R. Specificity of charge-carrying residues in the voltage sensor of potassium channels. J. Gen. Physiol. 2004, 123:205-216.
86. Seoh S.A., et al. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron 1996, 16:1159-1167.
87. Islas L.D., Sigworth F.J. Voltage sensitivity and gating charge in Shaker and Shab family potassium channels. J. Gen. Physiol. 1999, 114:723-742.