Gating-pore currents demonstrate selective and specific modulation of individual sodium channel voltage-sensors by biological toxins

Molecular Pharmacology

Volumn 86, Issue 2, 2014, Pages 159-167

  Xiao, Yucheng ^a   Blumenthal, Kenneth ^b   Cummins, Theodore R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOPLEURINE B; HUWENTOXIN IV; SEA ANEMONE TOXIN; SODIUM CHANNEL NAV1.5; SPIDER VENOM; UNCLASSIFIED DRUG;

ARTICLE; BIOSENSOR; CELL MEMBRANE POTENTIAL; CHANNEL GATING; DRUG MECHANISM; EMBRYO; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; MAMMAL CELL; PRIORITY JOURNAL; SODIUM CURRENT; TARANTULA;

CELL LINE; HEK293 CELLS; HUMANS; ION CHANNEL GATING; PEPTIDES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; TOXINS, BIOLOGICAL;

EID: 84903612446     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.092338     Document Type: Article

References (37)

1. Aldrich RW, Corey DP, and Stevens CF (1983) A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature 306:436-441. (Pubitemid 14235560)
2. Benzinger GR, Kyle JW, Blumenthal KM, and Hanck DA (1998) A specific interaction between the cardiac sodium channel and site-3 toxin anthopleurin B. J Biol Chem 273:80-84. (Pubitemid 28042179)
3. Bezanilla F (2008) How membrane proteins sense voltage. Nat Rev Mol Cell Biol 9:323-332.
4. Bezanilla F and Armstrong CM (1977) Inactivation of the sodium channel. I. Sodium current experiments. J Gen Physiol 70:549-566. (Pubitemid 8239321)
5. Blumenthal KM and Seibert AL (2003) Voltage-gated sodium channel toxins: poisons, probes, and future promise. Cell Biochem Biophys 38:215-238.
6. Bosmans F, Martin-Eauclaire MF, and Swartz KJ (2008) Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456:202-208.
7. Bosmans F, Rash L, Zhu S, Diochot S, Lazdunski M, Escoubas P, and Tytgat J (2006) Four novel tarantula toxins as selective modulators of voltage-gated sodium channel subtypes. Mol Pharmacol 69:419-429. (Pubitemid 43121939)
8. Capes DL, Arcisio-Miranda M, Jarecki BW, French RJ, and Chanda B (2012) Gating transitions in the selectivity filter region of a sodium channel are coupled to the domain IV voltage sensor. Proc Natl Acad Sci USA 109:2648-2653.
9. Capes DL, Goldschen-Ohm MP, Arcisio-Miranda M, Bezanilla F, and Chanda B (2013) Domain IV voltage-sensor movement is both sufficient and rate limiting for fast inactivation in sodium channels. J Gen Physiol 142:101-112.
10. Catterall WA (2002) Molecular mechanisms of gating and drug block of sodium channels. Novartis Found Symp 241:206-218, discussion 218-232.
11. Cestèle S and Catterall WA (2000) Molecular mechanisms of neurotoxin action on voltage-gated sodium channels. Biochimie 82:883-892.
12. Chen LQ, Santarelli V, Horn R, and Kallen RG (1996) A unique role for the S4 segment of domain 4 in the inactivation of sodium channels. J Gen Physiol 108:549-556. (Pubitemid 26427121)
13. Edgerton GB, Blumenthal KM, and Hanck DA (2008) Evidence for multiple effects of ProTxII on activation gating in Na(V)1.5. Toxicon 52:489-500.
14. Gallagher MJ and Blumenthal KM (1992) Cloning and expression of wild-type and mutant forms of the cardiotonic polypeptide anthopleurin B. J Biol Chem 267:13958-13963.
15. George AL, Jr (2005) Inherited disorders of voltage-gated sodium channels. J Clin Invest 115:1990-1999.
16. Lossin C, Wang DW, Rhodes TH, Vanoye CG, and George AL, Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34 :877-884. (Pubitemid 34722278)
17. Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao YD, and Garsky VM et al. (2002) Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 41:14734-14747. (Pubitemid 35470652)
18. Satin J, Kyle JW, Chen M, Bell P, Cribbs LL, Fozzard HA, and Rogart RB (1992) A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science 256:1202-1205.
19. 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.
20. Sheets MF, Kyle JW, Kallen RG, and Hanck DA (1999) The Na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophys J 77:747-757. (Pubitemid 29362449)
21. 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. (Pubitemid 40418418)
22. 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. (Pubitemid 47100615)
23. Sokolov S, Kraus RL, Scheuer T, and Catterall WA (2008a) Inhibition of sodium channel gating by trapping the domain II voltage sensor with protoxin II. Mol Pharmacol 73:1020-1028. (Pubitemid 351397907)
24. Sokolov S, Scheuer T, and Catterall WA (2005) Ion permeation through a voltage-sensitive gating pore in brain sodium channels having voltage sensor mutations. Neuron 47:183-189. (Pubitemid 41019250)
25. Sokolov S, Scheuer T, and Catterall WA (2007) Gating pore current in an inherited ion channelopathy. Nature 446:76-78. (Pubitemid 46348048)
26. Sokolov S, Scheuer T, and Catterall WA (2008b) Depolarization-activated gating pore current conducted by mutant sodium channels in potassium-sensitive normokalemic periodic paralysis. Proc Natl Acad Sci USA 105:19980-19985.
27. Sokolov S, Scheuer T, and Catterall WA (2010) Ion permeation and block of the gating pore in the voltage sensor of NaV1.4 channels with hypokalemic periodic paralysis mutations. J Gen Physiol 136:225-236.
28. Starace DM and Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427:548-553. (Pubitemid 38209113)
29. Struyk AF and Cannon SC (2007) A Na+ channel mutation linked to hypokalemic periodic paralysis exposes a proton-selective gating pore. J Gen Physiol 130:11-20. (Pubitemid 47001069)
30. Tombola F, Pathak MM, Gorostiza P, and Isacoff EY (2007) The twisted ion-permeation pathway of a resting voltage-sensing domain. Nature 445:546-549. (Pubitemid 46197635)
31. Tombola F, Pathak MM, and Isacoff EY (2005) Voltage-sensing arginines in a potassium channel permeate and occlude cation-selective pores. Neuron 45:379-388. (Pubitemid 40188206)
32. Waxman SG, Dib-Hajj S, Cummins TR, and Black JA (2000) Sodium channels and their genes: dynamic expression in the normal nervous system, dysregulation in disease states(1). Brain Res 886:5-14.
33. Wu F, Mi W, Burns DK, Fu Y, Gray HF, Struyk AF, and Cannon SC (2011) A sodium channel knockin mutant (NaV1.4-R669H) mouse model of hypokalemic periodic paralysis. J Clin Invest 121:4082-4094.
34. 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.
35. Xiao Y, Blumenthal K, Jackson JO, 2nd, Liang S, and Cummins TR (2010) The tarantula toxins ProTx-II and huwentoxin-IV differentially interact with human Nav1.7 voltage sensors to inhibit channel activation and inactivation. Mol Pharmacol 78:1124-1134.
36. Xiao Y, Jackson JO, 2nd, Liang S, and Cummins TR (2011) Common molecular determinants of tarantula huwentoxin-IV inhibition of Na+ channel voltage sensors in domains II and IV. J Biol Chem 286:27301-27310.
37. Yang YC and Kuo CC (2003) The position of the fourth segment of domain 4 determines status of the inactivation gate in Na+ channels. J Neurosci 23:4922-4930.