Importance of position 8 in μ-conotoxin KIIIA for voltage-gated sodium channel selectivity

FEBS Journal

Volumn 278, Issue 18, 2011, Pages 3408-3418

  Van Der Haegen, Annelies ^a   Peigneur, Steve ^a   Tytgat, Jan ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

conotoxins; Conus kinoshitai; electrophysiology; KIIIA; sodium channels

Indexed keywords

ARGININE; CONOTOXIN; GLUTAMIC ACID; GLUTAMINE; MU CONOTOXIN KIIIA; TRYPTOPHAN; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPOLARIZATION; DRUG POTENCY; NERVE CELL; NONHUMAN; OOCYTE; PHARMACOPHORE; PRIORITY JOURNAL; RECEPTOR BLOCKING; SKELETAL MUSCLE; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELLS, CULTURED; CONOTOXINS; DRUG DESIGN; HUMANS; KINETICS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; PROTEIN FOLDING; PROTEIN ISOFORMS; RATS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS;

XENOPUS LAEVIS;

EID: 80052503806     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08264.x     Document Type: Article

References (35)

1. Norton RS, &, Olivera BM, (2006) Conotoxins down under. Toxicon 48, 780-798.
2. Lewis RJ, (2004) Conotoxins as selective inhibitors of neuronal ion channels, receptors and transporters. IUBMB Life 56, 89-93.
3. Wang CZ, &, Chi CW, (2004) Conus peptides-a rich pharmaceutical treasure. Acta Biochim Biophys Sin (Shanghai) 36, 713-723.
4. Livett BG, Gayler KR, &, Khalil Z, (2004) Drugs from the sea: conopeptides as potential therapeutics. Curr Med Chem 11, 1715-1723.
5. Fiedler B, Zhang MM, Buczek O, Azam L, Bulaj G, Norton RS, Olivera BM, &, Yoshikami D, (2008) Specificity, affinity and efficacy of iota-conotoxin RXIA, an agonist of voltage-gated sodium channels Na(V)1.2, 1.6 and 1.7. Biochem Pharmacol 75, 2334-2344.
6. Ekberg J, Craik DJ, &, Adams DJ, (2008) Conotoxin modulation of voltage-gated sodium channels. Int J Biochem Cell Biol 40, 2363-2368.
7. Li RA, Ennis IL, French RJ, Dudley SC Jr, Tomaselli GF, &, Marban E, (2001) Clockwise domain arrangement of the sodium channel revealed by (mu)-conotoxin (GIIIA) docking orientation. J Biol Chem 276, 11072-11077.
8. Dudley SC Jr, Chang N, Hall J, Lipkind G, Fozzard HA, &, French RJ, (2000) mu-Conotoxin GIIIA interactions with the voltage-gated Na(+) channel predict a clockwise arrangement of the domains. J Gen Physiol 116, 679-690.
9. Stephan MM, Potts JF, &, Agnew WS, (1994) The microI skeletal muscle sodium channel: mutation E403Q eliminates sensitivity to tetrodotoxin but not to mu-conotoxins GIIIA and GIIIB. J Membr Biol 137, 1-8.
10. Bulaj G, West PJ, Garrett JE, Watkins M, Zhang MM, Norton RS, Smith BJ, Yoshikami D, &, Olivera BM, (2005) Novel conotoxins from Conus striatus and Conus kinoshitai selectively block TTX-resistant sodium channels. Biochemistry 44, 7259-7265.
11. Zhang MM, Green BR, Catlin P, Fiedler B, Azam L, Chadwick A, Terlau H, McArthur JR, French RJ, Gulyas J, et al. (2007) Structure/function characterization of micro-conotoxin KIIIA, an analgesic, nearly irreversible blocker of mammalian neuronal sodium channels. J Biol Chem 282, 30699-30706.
12. Zhang MM, Han TS, Olivera BM, Bulaj G, &, Yoshikami D, (2010) Mu-conotoxin KIIIA derivatives with divergent affinities versus efficacies in blocking voltage-gated sodium channels. Biochemistry 49, 4804-4812.
13. Han TS, Zhang MM, Walewska A, Gruszczynski P, Robertson CR, Cheatham TE 3rd, Yoshikami D, Olivera BM, &, Bulaj G, (2009) Structurally minimized mu-conotoxin analogues as sodium channel blockers: implications for designing conopeptide-based therapeutics. ChemMedChem 4, 406-414.
14. Khoo KK, Feng ZP, Smith BJ, Zhang MM, Yoshikami D, Olivera BM, Bulaj G, &, Norton RS, (2009) Structure of the analgesic mu-conotoxin KIIIA and effects on the structure and function of disulfide deletion. Biochemistry 48, 1210-1219.
15. Han TS, Zhang MM, Gowd KH, Walewska A, Yoshikami D, Olivera BM, &, Bulaj G, (2010) Disulfide-depleted selenoconopeptides: a minimalist strategy to oxidative folding of cysteine-rich peptides. ACS Med Chem Lett 1, 140-144.
16. Zhang MM, Gruszczynski P, Walewska A, Bulaj G, Olivera BM, &, Yoshikami D, (2010) Cooccupancy of the outer vestibule of voltage-gated sodium channels by micro-conotoxin KIIIA and saxitoxin or tetrodotoxin. J Neurophysiol 104, 88-97.
17. Zhang MM, McArthur JR, Azam L, Bulaj G, Olivera BM, French RJ, &, Yoshikami D, (2009) Synergistic and antagonistic interactions between tetrodotoxin and mu-conotoxin in blocking voltage-gated sodium channels. Channels (Austin) 3, 32-38.
18. Sato K, Ishida Y, Wakamatsu K, Kato R, Honda H, Ohizumi Y, Nakamura H, Ohya M, Lancelin JM, Kohda D, et al. (1991) Active site of mu-conotoxin GIIIA, a peptide blocker of muscle sodium channels. J Biol Chem 266, 16989-16991.
19. Becker S, Prusak-Sochaczewski E, Zamponi G, Beck-Sickinger AG, Gordon RD, &, French RJ, (1992) Action of derivatives of mu-conotoxin GIIIA on sodium channels. Single amino acid substitutions in the toxin separately affect association and dissociation rates. Biochemistry 31, 8229-8238.
20. Chahine M, Sirois J, Marcotte P, Chen L, &, Kallen RG, (1998) Extrapore residues of the S5-S6 loop of domain 2 of the voltage-gated skeletal muscle sodium channel (rSkM1) contribute to the mu-conotoxin GIIIA binding site. Biophys J 75, 236-246.
21. + channel mutant: possible localization of a binding site at the outer vestibule. Biophys J 69, 1657-1665.
22. + channels revealed by cysteine mutagenesis. Biophys J 73, 1874-1884.
23. + channel localized by mutant cycle analysis. Biochemistry 37, 4407-4419.
24. + channel domain I P-loop: implications for toxin-pore binding geometry. Biophys J 85, 2299-2310.
25. Choudhary G, Aliste MP, Tieleman DP, French RJ, &, Dudley SC Jr, (2007) Docking of mu-conotoxin GIIIA in the sodium channel outer vestibule. Channels (Austin) 1, 344-352.
26. Fuller E, Green BR, Catlin P, Buczek O, Nielsen JS, Olivera BM, &, Bulaj G, (2005) Oxidative folding of conotoxins sharing an identical disulfide bridging framework. FEBS J 272, 1727-1738.
27. Cummins TR, Aglieco F, &, Dib-Hajj SD, (2002) Critical molecular determinants of voltage-gated sodium channel sensitivity to mu-conotoxins GIIIA/B. Mol Pharmacol 61, 1192-1201.
28. Li RA, Ennis IL, Tomaselli GF, French RJ, &, Marban E, (2001) Latent specificity of molecular recognition in sodium channels engineered to discriminate between two 'indistinguishable' mu-conotoxins. Biochemistry 40, 6002-6008.
29. + channels. J Biol Chem 275, 27551-27558.
30. + channels. J Biol Chem 278, 8717-8724.
31. French RJ, Prusak-Sochaczewski E, Zamponi GW, Becker S, Kularatna AS, &, Horn R, (1996) Interactions between a pore-blocking peptide and the voltage sensor of the sodium channel: an electrostatic approach to channel geometry. Neuron 16, 407-413.
32. Hui K, Lipkind G, Fozzard HA, &, French RJ, (2002) Electrostatic and steric contributions to block of the skeletal muscle sodium channel by mu-conotoxin. J Gen Physiol 119, 45-54.
33. Ogiwara I, Ito K, Sawaishi Y, Osaka H, Mazaki E, Inoue I, Montal M, Hashikawa T, Shike T, Fujiwara T, et al. (2009) De novo mutations of voltage-gated sodium channel alphaII gene SCN2A in intractable epilepsies. Neurology 73, 1046-1053.
34. Meisler MH, O'Brien JE, &, Sharkey LM, (2010) Sodium channel gene family: epilepsy mutations, gene interactions and modifier effects. J Physiol 588, 1841-1848.
35. + channel determined by construction of multimeric cDNAs. Neuron 9, 861-871.