Toxin binding reveals two open state structures for one acid-sensing ion channel

Channels

Volumn 6, Issue 6, 2012, Pages 409-413

  Gründer, Stefan ^a   Augustinowski, Katrin ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

Acid sensing ion channel; ASIC; Desensitization; Ion selectivity; Pore structure

Indexed keywords

ACID SENSING ION CHANNEL; CATION; PSALMOTOXIN 1; SPIDER VENOM; UNCLASSIFIED DRUG;

CHICKEN; CONFORMATION; CRYSTAL STRUCTURE; DESENSITIZATION; MOLECULAR INTERACTION; NOTE; PH;

EID: 84871430580     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.22154     Document Type: Note

References (33)

1. Waldmann R, Champigny G, Bassilana F, Heurteaux C, Lazdunski M. A proton-gated cation channel involved in acid-sensing. Nature 1997; 386:173-7; PMID:9062189; http://dx.doi.org/10.1038/386173a0.
2. Deval E, Gasull X, Noël J, Salinas M, Baron A, Diochot S, et al. Acid-sensing ion channels (ASICs): pharmacology and implication in pain. Pharmacol Ther 2010; 128:549-58; PMID:20807551; http://dx.doi.org/10.1016/j. pharmthera.2010.08.006.
3. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, et al. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 2004; 118:687-98; PMID:15369669; http://dx.doi.org/10.1016/j.cell.2004.08.026.
4. Friese MA, Craner MJ, Etzensperger R, Vergo S, Wemmie JA, Welsh MJ, et al. Acid-sensing ion channel-1 contributes to axonal degeneration in autoimmune inflammation of the central nervous system. Nat Med 2007; 13:1483-9; PMID:17994101; http://dx.doi.org/10.1038/nm1668.
5. Jasti J, Furukawa H, Gonzales EB, Gouaux E. Structure of acid-sensing ion channel 1 at 1.9 A resolution and low pH. Nature 2007; 449:316-23; PMID:17882215; http://dx.doi.org/10.1038/nature06163.
6. Baconguis I, Gouaux E. Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 2012; 489:400-5; PMID:22842900; http://dx.doi.org/10.1038/nature11375.
7. Babini E, Paukert M, Geisler HS, Gründer S. Alternative splicing and interaction with di- and polyvalent cations control the dynamic range of acid-sensing ion channel 1 (ASIC1). J Biol Chem 2002; 277:41597-603; PMID:12198124; http://dx.doi.org/10.1074/jbc.M205877200.
8. Chen X, Kalbacher H, Gründer S. The tarantula toxin psalmotoxin 1 inhibits acid-sensing ion channel (ASIC) 1a by increasing its apparent H+ affinity. J Gen Physiol 2005; 126:71-9; PMID:15955877; http://dx.doi.org/10. 1085/jgp.200509303.
9. Escoubas P, De Weille JR, Lecoq A, Diochot S, Waldmann R, Champigny G, et al. Isolation of a tarantula toxin specific for a class of proton-gated Na+ channels. J Biol Chem 2000; 275:25116-21; PMID:10829030; http://dx.doi.org/10. 1074/jbc.M003643200.
10. Chen X, Kalbacher H, Gründer S. Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J Gen Physiol 2006; 127:267-76; PMID:16505147; http://dx.doi.org/10.1085/jgp. 200509409.
11. Samways DS, Harkins AB, Egan TM. Native and recombinant ASIC1a receptors conduct negligible Ca2+ entry. Cell Calcium 2009; 45:319-25; PMID:19185346; http://dx.doi.org/10.1016/j.ceca.2008.12.002.
12. Dawson RJ, Benz J, Stohler P, Tetaz T, Joseph C, Huber S, et al. Structure of the acid-sensing ion channel 1 in complex with the gating modifier Psalmotoxin 1. Nat Commun 2012; 3:936; PMID:22760635; http://dx.doi.org/10.1038/ ncomms1917.
13. Gonzales EB, Kawate T, Gouaux E. Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 2009; 460:599-604; PMID:19641589; http://dx.doi.org/10.1038/nature08218.
14. Pietra F. Docking and MD simulations of the interaction of the tarantula peptide psalmotoxin-1 with ASIC1a channels using a homology model. J Chem Inf Model 2009; 49:972-7; PMID:19309113; http://dx.doi.org/10.1021/ci800463h.
15. Qadri YJ, Berdiev BK, Song Y, Lippton HL, Fuller CM, Benos DJ. Psalmotoxin-1 docking to human acid-sensing ion channel-1. J Biol Chem 2009; 284:17625-33; PMID:19395383; http://dx.doi.org/10.1074/jbc.M109.003913.
16. Saez NJ, Mobli M, Bieri M, Chassagnon IR, Malde AK, Gamsjaeger R, et al. A dynamic pharmacophore drives the interaction between Psalmotoxin-1 and the putative drug target acid-sensing ion channel 1a. Mol Pharmacol 2011; 80:796-808; PMID:21825095; http://dx.doi.org/10.1124/mol.111.072207.
17. Lange A, Giller K, Hornig S, Martin-Eauclaire MF, Pongs O, Becker S, et al. Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 2006; 440:959-62; PMID:16612389; http://dx.doi.org/10. 1038/nature04649.
18. Escoubas P, Bernard C, Lambeau G, Lazdunski M, Darbon H. Recombinant production and solution structure of PcTx1, the specific peptide inhibitor of ASIC1a proton-gated cation channels. Protein Sci 2003; 12:1332-43; PMID:12824480; http://dx.doi.org/10.1110/ps.0307003.
19. Bourne Y, Talley TT, Hansen SB, Taylor P, Marchot P. Crystal structure of a Cbtx-AChBP complex reveals essential interactions between snake alpha-neurotoxins and nicotinic receptors. EMBO J 2005; 24:1512-22; PMID:15791209; http://dx.doi.org/10.1038/sj.emboj.7600620.
20. Celie PH, Kasheverov IE, Mordvintsev DY, Hogg RC, van Nierop P, van Elk R, et al. Crystal structure of nicotinic acetylcholine receptor homolog AChBP in complex with an alpha-conotoxin PnIA variant. Nat Struct Mol Biol 2005; 12:582-8; PMID:15951818; http://dx.doi.org/10.1038/nsmb951.
21. Hansen SB, Sulzenbacher G, Huxford T, Marchot P, Taylor P, Bourne Y. Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J 2005; 24:3635-46; PMID:16193063; http://dx.doi.org/10.1038/sj.emboj.7600828.
22. Dellisanti CD, Yao Y, Stroud JC, Wang ZZ, Chen L. Crystal structure of the extracellular domain of nAChR alpha1 bound to alpha-bungarotoxin at 1.94 A resolution. Nat Neurosci 2007; 10:953-62; PMID:17643119; http://dx.doi.org/10. 1038/nn1942.
23. Dutertre S, Lewis RJ. Toxin insights into nicotinic acetylcholine receptors. Biochem Pharmacol 2006; 72:661-70; PMID:16716265; http://dx.doi.org/10.1016/j.bcp.2006.03.027.
24. Gründer S, Chen X. Structure, function, and pharmacology of acid-sensing ion channels (ASICs): focus on ASIC1a. Int J Physiol Pathophysiol Pharmacol 2010; 2:73-94; PMID:21383888.
25. Springauf A, Gründer S. An acid-sensing ion channel from shark (Squalus acanthias) mediates transient and sustained responses to protons. J Physiol 2010; 588:809-20; PMID:20064854; http://dx.doi.org/10.1113/jphysiol. 2009.182931.
26. Wiemuth D, Gründer S. A single amino acid tunes Ca2+ inhibition of brain liver intestine Na+ channel (BLINaC). J Biol Chem 2010; 285:30404-10; PMID:20656685; http://dx.doi.org/10.1074/jbc.M110.153064.
27. Li T, Yang Y, Canessa CM. Outlines of the pore in open and closed conformations describe the gating mechanism of ASIC1. Nat Commun 2011; 2:399; PMID:21772270; http://dx.doi.org/10.1038/ncomms1409.
28. Dürrnagel S, Kuhn A, Tsiairis CD, Williamson M, Kalbacher H, Grimmelikhuijzen CJ, et al. Three homologous subunits form a high affinity peptide-gated ion channel in Hydra. J Biol Chem 2010; 285:11958-65; PMID:20159980; http://dx.doi.org/10.1074/jbc.M109.059998.
29. Li T, Yang Y, Canessa CM. Asn415 in the beta11-beta12 linker decreases proton-dependent desensitization of ASIC1. J Biol Chem 2010; 285:31285-91; PMID:20675379; http://dx.doi.org/10.1074/jbc.M110.160382.
30. Springauf A, Bresenitz P, Gründer S. The interaction between two extracellular linker regions controls sustained opening of acid-sensing ion channel 1. J Biol Chem 2011; 286:24374-84; PMID:21576243; http://dx.doi.org/10. 1074/jbc.M111.230797.
31. Cushman KA, Marsh-Haffner J, Adelman JP, McCleskey EW. A conformation change in the extracellular domain that accompanies desensitization of acid-sensing ion channel (ASIC) 3. J Gen Physiol 2007; 129:345-50; PMID:17389250; http://dx.doi.org/10.1085/jgp.200709757.
32. Lingueglia E, de Weille JR, Bassilana F, Heurteaux C, Sakai H, Waldmann R, et al. A modulatory subunit of acid sensing ion channels in brain and dorsal root ganglion cells. J Biol Chem 1997; 272:29778-83; PMID:9368048; http://dx.doi.org/10.1074/jbc.272.47.29778.
33. Immke DC, McCleskey EW. Protons open acid-sensing ion channels by catalyzing relief of Ca2+ blockade. Neuron 2003; 37:75-84; PMID:12526774; http://dx.doi.org/10.1016/S0896-6273(02)01130-3.