A surface plasmon resonance approach to monitor toxin interactions with an isolated voltage-gated sodium channel paddle motif

Journal of General Physiology

Volumn 145, Issue 2, 2015, Pages 155-162

  Martin Eauclaire, Marie France ^a   Ferracci, Géraldine ^a   Bosmans, Frank ^a,b   Bougis, Pierre E ^a  

^a University of Mediterranée   (France)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BINDING; SCN2A1 PROTEIN, RAT; SCORPION VENOM; SODIUM CHANNEL BLOCKING AGENT; SODIUM CHANNEL NAV1.2;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROCEDURES; PROTEIN MOTIF; RAT; SURFACE PLASMON RESONANCE; XENOPUS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; MOLECULAR SEQUENCE DATA; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; PROTEIN BINDING; RATS; SCORPION VENOMS; SODIUM CHANNEL BLOCKERS; SURFACE PLASMON RESONANCE; XENOPUS;

EID: 84921773678     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201411268     Document Type: Article

References (39)

1. Alabi, A.A., M.I. Bahamonde, H.J. Jung, J.I. Kim, and K.J. Swartz. 2007. Portability of paddle motif function and pharmacology in voltage sensors. Nature. 450:370-375. http://dx.doi.org/10.1038/nature06266
2. Bende, N.S., S. Dziemborowicz, M. Mobli, V. Herzig, J. Gilchrist, J. Wagner, G.M. Nicholson, G.F. King, and F. Bosmans. 2014. A distinct sodium channel voltage-sensor locus determines insect selectivity of the spider toxin Dc1a. Nat. Commun. 5:4350. http:// dx.doi.org/10.1038/ncomms5350
3. Bennett, P.B., K. Yazawa, N. Makita, and A.L. George Jr. 1995. Molecular mechanism for an inherited cardiac arrhythmia. Nature. 376:683-685. http://dx.doi.org/10.1038/376683a0
4. Benzinger, G.R., J.W. Kyle, K.M. Blumenthal, and D.A. Hanck. 1998. A specific interaction between the cardiac sodium channel and site-3 toxin anthopleurin B. J. Biol. Chem. 273:80-84. http://dx.doi.org/ 10.1074/jbc.273.1.80
5. Bezanilla, F. 2008. How membrane proteins sense voltage. Nat. Rev. Mol. Cell Biol. 9:323-332. http://dx.doi.org/10.1038/nrm2376
6. Bosmans, F., M.F. Martin-Eauclaire, and K.J. Swartz. 2008. Deconstructing voltage sensor function and pharmacology in sodium channels. Nature. 456:202-208. http://dx.doi.org/10.1038/ nature07473
7. Bosmans, F., M. Puopolo, M.F. Martin-Eauclaire, B.P. Bean, and K.J. Swartz. 2011. Functional properties and toxin pharmacology of a dorsal root ganglion sodium channel viewed through its voltage sensors. J. Gen. Physiol. 138:59-72. http://dx.doi.org/10.1085/jgp.201110614
8. Capes, D.L., M.P. Goldschen-Ohm, M. Arcisio-Miranda, F. Bezanilla, and B. Chanda. 2013. Domain IV voltage-sensor movement is both sufficient and rate limiting for fast inactivation in sodium channels. J. Gen. Physiol. 142:101-112. http://dx.doi.org/10.1085/jgp.201310998
9. Cestele, S., Y. Qu, J.C. Rogers, H. Rochat, T. Scheuer, and W.A. Catterall. 1998. Voltage sensor-trapping: Enhanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron. 21:919-931. http://dx.doi.org/10.1016/ S0896-6273(00)80606-6
10. Cestele, S., V. Yarov-Yarovoy, Y. Qu, F. Sampieri, T. Scheuer, and W.A. Catterall. 2006. Structure and function of the voltage sensor of sodium channels probed by a beta-scorpion toxin. J. Biol. Chem. 281:21332-21344. http://dx.doi.org/10.1074/jbc.M603814200
11. Chioni, A.M., S.P. Fraser, F. Pani, P. Foran, G.P. Wilkin, J.K.J. Diss, and M.B.A. Djamgoz. 2005. A novel polyclonal antibody specific for the Nav1.5 voltage-gated Na+ channel 'neonatal' splice form. J. Neurosci. Methods. 147:88-98. http://dx.doi.org/10.1016/j.jneumeth.2005.03.010
12. Crest, M., G. Jacquet, M. Gola, H. Zerrouk, A. Benslimane, H. Rochat, P. Mansuelle, and M.F. Martin-Eauclaire. 1992. Kaliotoxin, a novel peptidyl inhibitor of neuronal BK-type Ca2+-activated K+ channels characterized from Androctonus mauretanicus mauretanicus venom. J. Biol. Chem. 267:1640-1647.
13. Gilchrist, J., B.M. Olivera, and F. Bosmans. 2014. Animal toxins influence voltage-gated sodium channel function. Handbook Exp. Pharmacol. 221:203-229. http://dx.doi.org/10.1007/978-3-642-41588-3_10
14. Gur, M., R. Kahn, I. Karbat, N. Regev, J. Wang, W.A. Catterall, D. Gordon, and M. Gurevitz. 2011. Elucidation of the molecular basis of selective recognition uncovers the interaction site for the core domain of scorpion alpha-toxins on sodium channels. J. Biol. Chem. 286:35209-35217. http://dx.doi.org/10.1074/jbc.M111.259507
15. Kalia, J., M. Milescu, J. Salvatierra, J. Wagner, J.K. Klint, G.F. King, B.M. Olivera, and F. Bosmans. 2015. From foe to friend: Using animal toxins to investigate ion channel function. J. Mol. Biol. 427:158-175. http://dx.doi.org/10.1016/j.jmb.2014.07.027
16. Karbat, I., N. Ilan, J.Z. Zhang, L. Cohen, R. Kahn, M. Benveniste, T. Scheuer, W.A. Catterall, D. Gordon, and M. Gurevitz. 2010. Partial agonist and antagonist activities of a mutant scorpion beta-toxin on sodium channels. J. Biol. Chem. 285:30531-30538. http://dx.doi.org/10.1074/jbc.M110.150888
17. Lee, J.H., C.K. Park, G. Chen, Q. Han, R.G. Xie, T. Liu, R.R. Ji, and S.Y. Lee. 2014. A monoclonal antibody that targets a NaV1.7 channel voltage sensor for pain and itch relief. Cell. 157:1393-1404. http://dx.doi.org/10.1016/j.cell.2014.03.064
18. Leipold, E., A. Hansel, A. Borges, and S.H. Heinemann. 2006. Subtype specificity of scorpion beta-toxin Tz1 interaction with voltage-gated sodium channels is determined by the pore loop of domain 3. Mol. Pharmacol. 70:340-347.
19. Li-Smerin, Y., and K.J. Swartz. 2000. Localization and molecular determinants of the Hanatoxin receptors on the voltage-sensing domains of a K+ channel. J. Gen. Physiol. 115:673-684. http:// dx.doi.org/10.1085/jgp.115.6.673
20. Long, S.B., X. Tao, E.B. Campbell, and R. MacKinnon. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature. 450:376-382. http://dx.doi.org/10.1038/nature06265
21. Martin, M.F., L.G. Garcia y Perez, M. el Ayeb, C. Kopeyan, G. Bechis, E. Jover, and H. Rochat. 1987. Purification and chemical and biological characterizations of seven toxins from the Mexican scorpion, Centruroides suffusus suffusus. J. Biol. Chem. 262:4452-4459.
22. Martin-Eauclaire, M.F., and H. Rochat. 2000. Purification and characterization of scorpion toxins acting on voltage-sensitive Na+ channels. In Methods and Tools in Biosciences and Medicine. Springer, Basel. 152-168. http://dx.doi.org/10.1007/978-3-0348-8466-2_10
23. Murata, Y., H. Iwasaki, M. Sasaki, K. Inaba, and Y. Okamura. 2005. Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature. 435:1239-1243. http://dx.doi.org/10.1038/ nature03650
24. Neumann, T., H.D. Junker, K. Schmidt, and R. Sekul. 2007. SPRbased fragment screening: Advantages and applications. Curr. Top. Med. Chem. 7:1630-1642. http://dx.doi.org/10.2174/15680 2607782341073
25. Payandeh, J., T. Scheuer, N. Zheng, and W.A. Catterall. 2011. The crystal structure of a voltage-gated sodium channel. Nature. 475:353-358. http://dx.doi.org/10.1038/nature10238
26. Ramsey, I.S., M.M. Moran, J.A. Chong, and D.E. Clapham. 2006. A voltage-gated proton-selective channel lacking the pore domain. Nature. 440:1213-1216. http://dx.doi.org/10.1038/nature04700
27. Rogers, J.C., Y. Qu, T.N. Tanada, T. Scheuer, and W.A. Catterall. 1996. Molecular determinants of high affinity binding of alphascorpion 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. http://dx.doi.org/10.1074/jbc.271.27.15950
28. Sasaki, M., M. Takagi, and Y. Okamura. 2006. A voltage sensor-domain protein is a voltage-gated proton channel. Science. 312:589- 592. http://dx.doi.org/10.1126/science.1122352
29. Schuck, P., and H. Zhao. 2010. The role of mass transport limitation and surface heterogeneity in the biophysical characterization of macromolecular binding processes by SPR biosensing. Methods Mol. Biol. 627:15-54. http://dx.doi.org/10.1007/978-1-60761-670-2_2
30. Sudhof, T.C., and J.E. Rothman. 2009. Membrane fusion: Grappling with SNARE and SM proteins. Science. 323:474-477. http://dx.doi.org/10.1126/science.1161748
31. Swartz, K.J. 2008. Sensing voltage across lipid membranes. Nature. 456:891-897. http://dx.doi.org/10.1038/nature07620
32. Swartz, K.J., and R. MacKinnon. 1997. Hanatoxin modifies the gating of a voltage-dependent K+ channel through multiple binding sites. Neuron. 18:665-673. http://dx.doi.org/10.1016/S0896-6273(00)80306-2
33. Ulbricht, W. 2005. Sodium channel inactivation: Molecular determinants and modulation. Physiol. Rev. 85:1271-1301. http://dx.doi.org/10.1152/physrev.00024.2004
34. Unnerstale, S., J. Lind, E. Papadopoulos, and L. Maler. 2009. Solution structure of the HsapBK K+ channel voltage-sensor paddle sequence. Biochemistry. 48:5813-5821. http://dx.doi.org/10.1021/ bi9004599
35. Unnerstale, S., F. Madani, A. Graslund, and L. Maler. 2012. Membrane-perturbing properties of two Arg-rich paddle domains from voltage-gated sensors in the KvAP and HsapBK K+ channels. Biochemistry. 51:3982-3992. http://dx.doi.org/10.1021/bi300188t
36. Wan, X., S. Chen, A. Sadeghpour, Q. Wang, and G.E. Kirsch. 2001. Accelerated inactivation in a mutant Na+ channel associated with idiopathic ventricular fibrillation. Am. J. Physiol. Heart Circ. Physiol. 280:H354-H360.
37. + channel voltage sensor. Proc. Natl. Acad. Sci. USA. 108:15426-15431. http://dx.doi.org/10.1073/pnas.1112320108
38. Zhang, J.Z., V. Yarov-Yarovoy, T. Scheuer, I. Karbat, L. Cohen, D. Gordon, M. Gurevitz, and W.A. Catterall. 2011. Structure-function map of the receptor site for β-scorpion toxins in domain II of voltage-gated sodium channels. J. Biol. Chem. 286:33641-33651. http://dx.doi.org/10.1074/jbc.M111.282509
39. Zhang, J.Z., V. Yarov-Yarovoy, T. Scheuer, I. Karbat, L. Cohen, D. Gordon, M. Gurevitz, and W.A. Catterall. 2012. Mapping the interaction site for a β-scorpion toxin in the pore module of domain III of voltage-gated Na+ channels. J. Biol. Chem. 287:30719- 30728. http://dx.doi.org/10.1074/jbc.M112.370742