The tarantula toxins ProTx-II and huwentoxin-IV differentially interact with human Nav1.7 voltage sensors to inhibit channel activation and inactivation

Molecular Pharmacology

Volumn 78, Issue 6, 2010, Pages 1124-1134

  Xiao, Yucheng ^a,c   Blumenthal, Kenneth ^b   Jackson II, James O ^a   Liang, Songping ^c   Cummins, Theodore R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c HUNAN NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTINE; HUWENTOXIN IV; PEPTIDE; PROTX 2; SODIUM CHANNEL NAV1.7; SPIDER VENOM; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; ELECTRIC POTENTIAL; ELECTRONIC SENSOR; IC 50; MUTATION; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; ANIMALS; FEMALE; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; SPIDER VENOMS; SPIDERS;

EID: 78649959796     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.066332     Document Type: Article

References (32)

1. Bendahhou S, Cummins TR, Kwiecinski H, Waxman SG, and Ptácek LJ (1999) Characterization of a new sodium channel mutation at arginine 1448 associated with moderate Paramyotonia congenita in humans. J Physiol 518:337-344.
2. Bosmans F, Martin-Eauclaire MF, and Swartz KJ (2008) Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456:202-208.
3. Catterall WA, Goldin AL, Waxman SG, and International Union of Pharmacology (2003) International Union of Pharmacology. XXXIX. Compendium of voltage-gated ion channels: sodium channels. Pharmacol Rev 55:575-578.
4. Cestèle S and Catterall WA (2000) Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82:883-892.
5. Cestèle S, Scheuer T, Mantegazza M, Rochat H, and Catterall WA (2001) Neutralization of gating charges in domain II of the sodium channel alpha subunit enhances voltage-sensor trapping by a beta-scorpion toxin. J Gen Physiol 118:291-302.
6. Cha A, Ruben PC, George AL, Jr., Fujimoto E, and Bezanilla F (1999) Voltage sensors in domains III and IV, but not I and II, are immobilized by Na+ channel fast inactivation. Neuron 22:73-87.
7. Chatelier A, Dahllund L, Eriksson A, Krupp J, and Chahine M (2008) Biophysical properties of human Na v1.7 splice variants and their regulation by protein kinase A. J Neurophysiol 99:2241-2250.
8. Cox JJ, Reimann F, Nicholas AK, Thornton G, Roberts E, Springell K, Karbani G, Jafri H, Mannan J, Raashid Y, et al. (2006) An SCN9A channelopathy causes congenital inability to experience pain. Nature 444:894-898.
9. v1.3 sodium channels: rapid repriming and slow closed-state inactivation display quantitative differences after expression in a mammalian cell line and in spinal sensory neurons. J Neurosci 21:5952-5961.
10. Cummins TR and Rush AM (2007) Voltage-gated sodium channel blockers for the treatment of neuropathic pain. Expert Rev Neurother 7:1597-1612.
11. Cummins TR, Sheets PL, and Waxman SG (2007) The roles of sodium channels in nociception: Implications for mechanisms of pain. Pain 131:243-257.
12. Klugbauer N, Lacinova L, Flockerzi V, and Hofmann F (1995) Structure and functional expression of a new member of the tetrodotoxin-sensitive voltage-activated sodium channel family from human neuroendocrine cells. EMBO J 14:1084-1090.
13. Leipold E, Lu S, Gordon D, Hansel A, and Heinemann SH (2004) Combinatorial interaction of scorpion toxins Lqh-2, Lqh-3, and LqhalphaIT with sodium channel receptor sites-3. Mol Pharmacol 65:685-691.
14. Lossin C, Wang DW, Rhodes TH, Vanoye CG, and George AL Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884.
15. v1.7 by OD1, a toxin from the scorpion Odonthobuthus doriae. Mol Pharmacol 70:405-414.
16. Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao YD, Garsky VM, et al. (2002) Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 41:14734-14747.
17. O'Leary ME (1998) Characterization of the isoform-specific differences in the gating of neuronal and muscle sodium channels. Can J Physiol Pharmacol 76:1041-1050.
18. Peng K, Shu Q, Liu Z, and Liang S (2002) Function and solution structure of huwentoxin-IV, a potent neuronal tetrodotoxin (TTX)-sensitive sodium channel antagonist from Chinese bird spider Selenocosmia huwena. J Biol Chem 277:47564-47571.
19. Raymond CK, Castle J, Garrett-Engele P, Armour CD, Kan Z, Tsinoremas N, and Johnson JM (2004) Expression of alternatively spliced sodium channel alphasubunit genes. Unique splicing patterns are observed in dorsal root ganglia. J Biol Chem 279:46234-46241.
20. Rogers JC, Qu Y, Tanada TN, Scheuer T, and Catterall WA (1996) Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit. J Biol Chem 271:15950-15962.
21. Schmalhofer WA, Calhoun J, Burrows R, Bailey T, Kohler MG, Weinglass AB, Kaczorowski GJ, Garcia ML, Koltzenburg M, and Priest BT (2008) ProTx-II, a selective inhibitor of NaV1.7 sodium channels, blocks action potential propagation in nociceptors. Mol Pharmacol 74:1476-1484.
22. Schmidt D and MacKinnon R (2008) Voltage-dependent K+ channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc Natl Acad Sci USA 105:19276-19281.
23. Sheets MF and Hanck DA (2007) Outward stabilization of the S4 segments in domains III and IV enhances lidocaine block of sodium channels. J Physiol 582:317-334.
24. Smith JJ, Alphy S, Seibert AL, and Blumenthal KM (2005) Differential phospholipid binding by site 3 and site 4 toxins. Implications for structural variability between voltage-sensitive sodium channel domains. J Biol Chem 280:11127-11133.
25. Smith JJ, Cummins TR, Alphy S, and Blumenthal KM (2007) 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 282:12687-12697.
26. Sokolov S, Kraus RL, Scheuer T, and Catterall WA (2008) Inhibition of sodium channel gating by trapping the domain II voltage sensor with protoxin II. Mol Pharmacol 73:1020-1028.
27. Strichartz GR and Wang GK (1986) Rapid voltage-dependent dissociation of scorpion alpha-toxins coupled to Na channel inactivation in amphibian myelinated nerves. J Gen Physiol 88:413-435.
28. Ukomadu C, Zhou J, Sigworth FJ, and Agnew WS (1992) muI Na+ channels expressed transiently in human embryonic kidney cells: biochemical and biophysical properties. Neuron 8:663-676.
29. Xiao Y, Bingham JP, Zhu W, Moczydlowski E, Liang S, and Cummins TR (2008) 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 283:27300-27313.
30. Xiao Y, Li J, Deng M, Dai C, and Liang S (2007) Characterization of the excitatory mechanism induced by Jingzhaotoxin-I inhibiting sodium channel inactivation. Toxicon 50:507-517.
31. Xiao Y, Tang J, Hu W, Xie J, Maertens C, Tytgat J, and Liang S (2005) Jingzhaotoxin-I, a novel spider neurotoxin preferentially inhibiting cardiac sodium channel inactivation. J Biol Chem 280:12069-12076. (Pubitemid 40491016)
32. Yang N, Ji S, Zhou M, Ptácek LJ, Barchi RL, Horn R, and George AL Jr (1994) Sodium channel mutations in paramyotonia congenita exhibit similar biophysical phenotypes in vitro. Proc Natl Acad Sci USA 91:12785-12789.