Aromatic amino acids in the finger domain of the FMRFamide-gated Na[Formula: see text] channel are involved in the FMRFamide recognition and the activation.
DEG/ENaC
Docking simulation
Dose-response
FMRFamide
FaNaC
Mutagenesis
Journal
Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
06
02
2023
accepted:
20
04
2023
revised:
18
04
2023
medline:
21
7
2023
pubmed:
8
6
2023
entrez:
8
6
2023
Statut:
ppublish
Résumé
FMRFamide-gated Na[Formula: see text] channel (FaNaC) is a member of the DEG/ENaC family and activated by a neuropeptide, FMRFamide. Structural information about the FMRFamide-dependent gating is, however, still elusive. Because two phenylalanines of FMRFamide are essential for the activation of FaNaC, we hypothesized that aromatic-aromatic interaction between FaNaC and FMRFamide is critical for FMRFamide recognition and/or the activation gating. Here, we focused on eight conserved aromatic residues in the finger domain of FaNaCs and tested our hypothesis by mutagenic analysis and in silico docking simulations. The mutation of conserved aromatic residues in the finger domain reduced the FMRFamide potency, suggesting that the conserved aromatic residues are involved in the FMRFamide-dependent activation. The kinetics of the FMRFamide-gated currents were also modified substantially in some mutants. Some results of docking simulations were consistent with a hypothesis that the aromatic-aromatic interaction between the aromatic residues in FaNaC and FMRFamide is involved in the FMRFamide recognition. Collectively, our results suggest that the conserved aromatic residues in the finger domain of FaNaC are important determinants of the ligand recognition and/or the activation gating in FaNaC.
Identifiants
pubmed: 37289212
doi: 10.1007/s00424-023-02817-9
pii: 10.1007/s00424-023-02817-9
doi:
Substances chimiques
Sodium Channels
0
FMRFamide
64190-70-1
Amino Acids, Aromatic
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
975-993Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Askwith CC, Cheng C, Ikuma M, Benson C, Price MP, Welsh MJ (2000) Neu-ropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/ENaC channels. Neuron 26:133–141. https://doi.org/10.1016/s0896-6273(00)81144-7
doi: 10.1016/s0896-6273(00)81144-7
pubmed: 10798398
Baconguis I, Gouaux E (2012) Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 489(7416):400–405. https://doi.org/10.1038/nature11375
doi: 10.1038/nature11375
pubmed: 22842900
pmcid: 3725952
Baconguis I, Bohlen CJ, Goehring A, Julius D, Gouaux E (2014) X-ray structure of acid-sensing ion channel 1-snake toxin complex reveals open state of a Na+-selective channel. Cell 156(4):717–729. https://doi.org/10.1016/j.cell.2014.01.011
doi: 10.1016/j.cell.2014.01.011
pubmed: 24507937
pmcid: 4190031
Bargeton B, Iwaszkiewicz J, Bonifacio G, Roy S, Zoete V, Kellenberger S (2019) Mutations in the palm domain disrupt modulation of acid-sensing ion channel 1a currents by neuropeptides. Sci Rep 9(1):2599. https://doi.org/10.1038/s41598-018-37426-5
doi: 10.1038/s41598-018-37426-5
pubmed: 30796301
pmcid: 6385203
Bohlen CJ, Chesler AT, Sharif-Naeini R, Medzihradszky KF, Zhou S, King D, Sánchez EE, Burlingame AL, Basbaum AI, Julius D (2011) A heteromeric Texas coral snake toxin targets acid-sensing ion channels to produce pain. Nature 479(7373):410–414. https://doi.org/10.1038/nature10607
doi: 10.1038/nature10607
pubmed: 22094702
pmcid: 3226747
Bonifacio G, Lelli CI, Kellenberger S (2014) Protonation controls ASIC1a activity via coordinated movements in multiple domains. J. Gen. Physiol. 143(1):105–118. https://doi.org/10.1085/jgp.201311053
doi: 10.1085/jgp.201311053
pubmed: 24344244
pmcid: 3874563
Catarsi S, Babinski K, Seguela P (2001) Selective modulation of heteromeric ASIC proton-gated channels by neuropeptide FF. Neuropharmacology 41(5):592–600. https://doi.org/10.1016/s0028-3908(01)00107-1
doi: 10.1016/s0028-3908(01)00107-1
pubmed: 11587714
Chen X, Kalbacher H, Gründer S (2006) Interaction of acid-sensing ion channel (ASIC) 1 with the tarantula toxin psalmotoxin 1 is state dependent. J. Gen. Physiol. 127(3):267–276. https://doi.org/10.1085/jgp.200509409
doi: 10.1085/jgp.200509409
pubmed: 16505147
pmcid: 2151504
Colquhoun D (1998) Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol. 125(5):924–947. https://doi.org/10.1038/sj.bjp.0702164
doi: 10.1038/sj.bjp.0702164
pubmed: 9846630
Cottrell GA (1997) The rst peptide-gated ion channel. J. Exp. Biol. 200(Pt 18):2377–2386. https://doi.org/10.1242/jeb.200.18.2377
doi: 10.1242/jeb.200.18.2377
pubmed: 9343851
Cottrell GA (2005) Domain near TM1 inuences agonist and antagonist responses of peptide-gated Na+ channels. Pflügers Arch. 450(3):168–177. https://doi.org/10.1007/s00424-005-1385-7
doi: 10.1007/s00424-005-1385-7
pubmed: 15843991
Cottrell GA, Green KA, Davies NW (1990) The neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) can activate a ligand-gated ion channel in Helix neurones. Plügers Arch. 416(5):612–614. https://doi.org/10.1007/BF00382698
doi: 10.1007/BF00382698
Cottrell GA, Jeziorski MC, Green KA (2001) Location of a ligand recognition site of FMRFamide-gated Na+ channels. FEBS Lett. 489(1):71–74. https://doi.org/10.1016/s0014-5793(01)02081-6
doi: 10.1016/s0014-5793(01)02081-6
pubmed: 11231016
Dandamudi M, Hausen H, Lynagh T (2022) Comparative analysis defines a broader FMRFamide-gated sodium channel family and determinants of neuropeptide sensi- tivity. J Biol Chem 298(7):102086. https://doi.org/10.1016/j.jbc.2022.102086
doi: 10.1016/j.jbc.2022.102086
pubmed: 35636513
pmcid: 9234716
Dawson RJ, Benz J, Stohler P, Tetaz T, Joseph C, Huber S, Schmid G, Hügin D, Pimlin P, Trube G, Rudolph MG, Hennig M, Ruf A (2012) Structure of the acid-sensing ion channel 1 in complex with the gating modi er Psalmotoxin 1. Nat Commun 3:936. https://doi.org/10.1038/ncomms1917
Dürrnagel S, Kuhn A, Tsiairis CD, Williamson M, Kalbacher H, Grimmelikhuijzen CJ, Holstein TW, Gründer S (2010) Three homologous subunits form a high affinity peptide-gated ion channel in Hydra. J. Biol. Chem. 285(16):11958–11965. https://doi.org/10.1074/jbc.M109.059998
doi: 10.1074/jbc.M109.059998
pubmed: 20159980
pmcid: 2852933
Dürrnagel S, Falkenburger BH, Gründer S (2012) High Ca2+ permeability of a peptide-gated DEG/ENaC from Hydra. J. Gen. Physiol. 140(4):391–402. https://doi.org/10.1085/jgp.201210798
doi: 10.1085/jgp.201210798
pubmed: 23008433
pmcid: 3457691
Feyfant E, Šali A, Fiser A (2007) Modeling mutations in protein structures. Protein Sci. 16(9):2030–2041. https://doi.org/10.1110/ps.072855507
doi: 10.1110/ps.072855507
pubmed: 17766392
pmcid: 2206969
Fujimoto A, Kodani Y, Furukawa Y (2017) Modulation of the FMRFamide-gated Na+ channel by external Ca2+. Pflügers Arch. 469(10):1335–1347. https://doi.org/10.1007/s00424-017-2021-z
doi: 10.1007/s00424-017-2021-z
pubmed: 28674755
Furukawa Y, Miyawaki Y, Abe G (2006) Molecular cloning and functional charac-terization of the Aplysia FMRFamide-gated Na+ channel. Pflügers Arch. 451(5):646–656. https://doi.org/10.1007/s00424-005-1498-z
doi: 10.1007/s00424-005-1498-z
pubmed: 16133260
Golubovic A, Kuhn A, Williamson M, Kalbacher H, Holstein TW, Grimmelikhuijzen CJ, Gründer S (2007) A peptide-gated ion channel from the freshwater polyp Hydra. J. Biol. Chem. 282(48):35098–35103. https://doi.org/10.1074/jbc.M706849200
doi: 10.1074/jbc.M706849200
pubmed: 17911098
Green KA, Cottrell GA (1999) Block of the Helix FMRFamide-gated Na+ chan-nel by FMRFamide and its analogues. Journal of Physiology 519:47–56. https://doi.org/10.1111/j.1469-7793.1999.0047o.x
doi: 10.1111/j.1469-7793.1999.0047o.x
pubmed: 10432338
pmcid: 2269487
Green KA, Cottrell GA (2002) Activity modes and modulation of the peptide-gated Na+ channel of Helix neurones. Pflügers Arch. 443(5–6):813–821. https://doi.org/10.1007/s00424-001-0750-4
doi: 10.1007/s00424-001-0750-4
pubmed: 11889580
Gründer S, Ramirez AO, Jekely G (2022) Neuropeptides and degenerin/epithelial Na+ channels: a relationship from mammals to cnidarians. J Physiol, online. https://doi.org/10.1113/JP282309
doi: 10.1113/JP282309
Hanukoglu I, Hanukoglu A (2016) Epithelial sodium channel (ENaC) family: Phy-logeny, structure-function, tissue distribution, and associated inherited diseases. Gene 579(2):95–132. https://doi.org/10.1016/j.gene.2015.12.061
doi: 10.1016/j.gene.2015.12.061
pubmed: 26772908
pmcid: 4756657
Jasti J, Furukawa H, Gonzales EB, Gouaux E (2007) Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449(7160):316–323. https://doi.org/10.1038/nature06163
doi: 10.1038/nature06163
pubmed: 17882215
Jeziorski MC, Green KA, Sommerville J, Cottrell GA (2000) Cloning and expression of a FMRFamide-gated Na+ channel from Helisoma trivolvis and comparison with the 38 native neuronal channel. J. Physiol. (Lond.) 526(Pt 1):13–25. https://doi.org/10.1111/j.1469-7793.2000.00013.x
doi: 10.1111/j.1469-7793.2000.00013.x
pubmed: 10878095
Jones MV, Westbrook GL (1995) Desensitized states prolong GABAA channel responses to brief agonist pulses. Neuron 15(1):181–191. https://doi.org/10.1016/0896-6273(95)90075-6
doi: 10.1016/0896-6273(95)90075-6
pubmed: 7542462
Jumper J et al (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596(7873):583–589. https://doi.org/10.1038/s41586-021-03819-2
doi: 10.1038/s41586-021-03819-2
pubmed: 34265844
pmcid: 8371605
Kellenberger S, Schild L (2002) Epithelial sodium channel/degenerin family of ion channels: A variety of functions for a shared structure. Physiological Review 82:735–767. https://doi.org/10.1152/physrev.00007.2002
doi: 10.1152/physrev.00007.2002
Kleyman TR, Carattino MD, Hughey RP (2009) ENaC at the cutting edge: regula-tion of epithelial sodium channels by proteases. J. Biol. Chem. 284(31):20447–20451. https://doi.org/10.1074/jbc.R800083200
doi: 10.1074/jbc.R800083200
pubmed: 19401469
pmcid: 2742807
Kodani Y, Furukawa Y (2010) Position 552 in a FMRFamide-gated Na+ channel affects the gating properties and the potency of FMRFamide. Zool. Sci. 27(5):440–448. https://doi.org/10.2108/zsj.27.440
doi: 10.2108/zsj.27.440
Kodani Y, Furukawa Y (2014) Electrostatic charge at position 552 affects the ac-tivation and permeation of FMRFamide-gated Na+ channels. J Physiol Sci 64(2):141–150. https://doi.org/10.1007/s12576-013-0303-6
doi: 10.1007/s12576-013-0303-6
pubmed: 24415456
Krauson AJ, Carattino MD (2016) The thumb domain mediates acid-sensing ion channel desensitization. J. Biol. Chem. 291(21):11407–11419. https://doi.org/10.1074/jbc.M115.702316
doi: 10.1074/jbc.M115.702316
pubmed: 27015804
pmcid: 4900284
Lamiable A, Thávenet P, Rey J, Vavrusa M, Derreumaux P, Tuffáry P (2016) PEP-FOLD3: faster de novo structure prediction for linear peptides in solution and in complex. Nucleic Acids Res. 44(W1):W449-454. https://doi.org/10.1093/nar/gkw329
doi: 10.1093/nar/gkw329
pubmed: 27131374
pmcid: 4987898
Lingueglia E, Champigny G, Lazdunski M, Barbry P (1995) Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature 378(6558):730–733. https://doi.org/10.1038/378730a0
doi: 10.1038/378730a0
pubmed: 7501021
Lingueglia E, Deval E, Lazdunski M (2006) FMRFamide-gated sodium channel and ASIC channels: a new class of ionotropic receptors for FMRFamide and related peptides. Peptides 27(5):1138–1152. https://doi.org/10.1016/j.peptides.2005.06.037
doi: 10.1016/j.peptides.2005.06.037
pubmed: 16516345
Niu YY, Yang Y, Liu Y, Huang LD, Yang XN, Fan YZ, Cheng XY, Cao P, Hu YM, Li L, Lu XY, Tian Y, Yu Y (2016) Exploration of the peptide recognition of an amiloride-sensitive FMRFamide peptide-gated sodium channel. J. Biol. Chem. 291(14):7571–7582. https://doi.org/10.1074/jbc.M115.710251
doi: 10.1074/jbc.M115.710251
pubmed: 26867576
pmcid: 4817185
Noreng S, Bharadwaj A, Posert R, Yoshioka C, Baconguis I (2018) Structure of the human epithelial sodium channel by cryo-electron microscopy. Elife 7:e39340. https://doi.org/10.7554/eLife.39340
doi: 10.7554/eLife.39340
pubmed: 30251954
pmcid: 6197857
Perry SJ, Straub VA, Schoeld MG, Burke JF, Benjamin PR (2001) Neuronal expression of an FMRFamide-gated Na+ channel and its modulation by acid pH. J. Neurosci. 21(15):5559–5567. https://doi.org/10.1523/JNEUROSCI.21-15-05559.2001
doi: 10.1523/JNEUROSCI.21-15-05559.2001
pubmed: 11466427
pmcid: 6762646
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Fer-rin TE (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. https://doi.org/10.1002/jcc.20084
doi: 10.1002/jcc.20084
pubmed: 15264254
R Development Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, 2011. https://www.R-project.org/ ISBN 3-900051-07-0
Reiners M, Margreiter MA, Oslender-Bujotzek A, Rossetti G, Gründer S, Schmidt A (2018) The Conorfamide RPRFa Stabilizes the Open Conformation of Acid-Sensing Ion Channel 3 via the Nonproton Ligand-Sensing Domain. Mol Pharmacol 94(4):1114–1124. https://doi.org/10.1124/mol.118.112375
doi: 10.1124/mol.118.112375
pubmed: 30012583
Šali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234(3):779–815. https://doi.org/10.1006/jmbi.1993.1626
doi: 10.1006/jmbi.1993.1626
pubmed: 8254673
Schmidt A, Bauknecht P, Williams EA, Augustinowski K, Gründer S, Jékely G (2018) Dual signaling of Wamide myoinhibitory peptides through a peptide-gated channel and a GPCR in Platynereis. FASEB J. 32(10):5338–5349. https://doi.org/10.1096/fj.201800274R
doi: 10.1096/fj.201800274R
pubmed: 29688813
Schrödinger, LLC. The PyMOL molecular graphics system, version 1.8. November 2015
Sherwood TW, Frey EN, Askwith CC (2012) Structure and activity of the acid-sensing ion channels. Am. J. Physiol., Cell Physiol. 303(7):699–710. https://doi.org/10.1152/ajpcell.00188.2012
doi: 10.1152/ajpcell.00188.2012
Stefani E, Bezanilla F (1998) Cut-open oocyte voltage-clamp technique. Methods Enzymol 293:300–318. https://doi.org/10.1016/s0076-6879(98)93020-8
doi: 10.1016/s0076-6879(98)93020-8
pubmed: 9711615
Taglialatela M, Toro L, Stefani E (1992) Novel voltage clamp to record small, fast currents from ion channels expressed in Xenopus oocytes. Biophys J 61(1):78–82. https://doi.org/10.1016/S0006-3495(92)81817-9
doi: 10.1016/S0006-3495(92)81817-9
pubmed: 1311612
pmcid: 1260224
Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31(2):455–461. https://doi.org/10.1002/jcc.21334
doi: 10.1002/jcc.21334
pubmed: 19499576
pmcid: 3041641
Velankar S, Alhroub Y, Alili A, Best C, Boutselakis HC, Caboche S, Conroy MJ, Dana JM, van Ginkel G, Golovin A, Gore SP, Gutmanas A, Haslam P, Hirshberg M, John M, Lagerstedt I, Mir S, Newman LE, Oldfield TJ, Penkett CJ, Pineda-Castillo J, Rinaldi L, Sahni G, Sawka G, Sen S, Slowley R, Sousa da Silva AW, Suarez-Uruena A, Swaminathan GJ, Symmons MF, Vranken WF, Wainwright M, Kleywegt GJ (2011) PDBe: Protein Data Bank in Europe. Nucleic Acids Res. 39(Database issue):D402–410. https://doi.org/10.1093/nar/gkq985
Xie J, Price MP, Wemmie JA, Askwith CC, Welsh MJ (2003) ASIC3 and ASIC1 mediate FMRFamide-related peptide enhancement of H+-gated currents in cultured dorsal root ganglion neurons. Journal of Neurophysiology 89:2459–2465. https://doi.org/10.1152/jn.00707.2002
Yang H, Yu Y, Li WG, Yu F, Cao H, Xu TL, Jiang H (2009) Inherent dynamics of the acid-sensing ion channel 1correlates with the gating mechanism. PLoS Biol. 7(7):e1000151. https://doi.org/10.1371/journal.pbio.1000151
Yoder N, Yoshioka C, Gouaux E (2018) Gating mechanisms of acid-sensing ion channels. Nature 555(7696):397–401. https://doi.org/10.1038/nature25782
doi: 10.1038/nature25782
pubmed: 29513651
pmcid: 5966032
Zhainazarov AB, Cottrell GA (1998) Single-channel currents of a peptide-gated sodium channel expressed in Xenopus oocytes. J. Physiol. (Lond.) 513(Pt 1):19–31. https://doi.org/10.1111/j.1469-7793.1998.019by.x
doi: 10.1111/j.1469-7793.1998.019by.x
pubmed: 9782156
Zhao B, Rassendren F, Kaang BK, Furukawa Y, Kubo T, Kandel ER (1994) A new class of noninactivating K+ channels from aplysia capable of contributing to the resting potential and ring patterns of neurons. Neuron 13(5):1205–1213. https://doi.org/10.1016/0896-6273(94)90058-2
doi: 10.1016/0896-6273(94)90058-2
pubmed: 7946357