Binary architecture of the Nav 1.2-β2 signaling complex

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Das, Samir ^a   Gilchrist, John ^b   Bosmans, Frank ^b   Van Petegem, Filip ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

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

Author keywords

[No Author keywords available]

Indexed keywords

ARCHITECTURE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CRYSTAL STRUCTURE; DISULFIDE BOND; GENE MUTATION; GENETIC SUSCEPTIBILITY; MUTAGENESIS; SCORING SYSTEM; SIGNAL TRANSDUCTION; CHEMISTRY; DNA MUTATIONAL ANALYSIS; HUMAN; METABOLISM; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN SUBUNIT; X RAY CRYSTALLOGRAPHY;

PROTEIN BINDING; PROTEIN SUBUNIT; SODIUM CHANNEL NAV1.2;

CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; HUMANS; NAV1.2 VOLTAGE-GATED SODIUM CHANNEL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN SUBUNITS;

EID: 84961262752     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10960     Document Type: Article

References (70)

1. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallographica Section D Biological Crystallography 66:213-221. doi:10.1107/S0907444909052925
2. Baum L, Haerian BS, Ng H-K, Wong VCN, Ng PW, Lui CHT, Sin NC, Zhang C, Tomlinson B, Wong GW-K, Tan HJ, Raymond AA, Mohamed Z, Kwan P. 2014. Case-control association study of polymorphisms in the voltage-gated sodium channel genes SCN1A, SCN2A, SCN3A, SCN1B, and SCN2B and epilepsy. Human Genetics 133: 651-659. doi:10.1007/s00439-013-1405-1
3. Bosmans F, Martin-Eauclaire MF, Swartz KJ. 2008. Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456:202-208. doi:10.1038/nature07473
4. Brackenbury WJ, Djamgoz MBA, Isom LL. 2008. An emerging role for voltage-gated Na+ channels in cellular migration: regulation of central nervous system development and potentiation of invasive cancers. The Neuroscientist 14:571-583. doi:10.1177/1073858408320293
5. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallographica. Section D, Biological Crystallography 54:905-921.
6. Calhoun JD, Isom LL. 2014. The role of non-pore-forming beta subunits in physiology and pathophysiology of voltage-gated sodium channels. Handbook of Experimental Pharmacology 221:51-89. doi:10.1007/978-3-642-41588-3_4
7. Capes DL, Goldschen-Ohm MP, Arcisio-Miranda M, Bezanilla F, Chanda B. 2013. Domain IV voltage-sensor movement is both sufficient and rate limiting for fast inactivation in sodium channels. The Journal of General Physiology 142:101-112. doi:10.1085/jgp.201310998
8. Catterall WA. 2012. Voltage-gated sodium channels at 60: structure, function and pathophysiology. The Journal of Physiology 590:2577-2589. doi:10.1113/jphysiol.2011.224204
9. Chanda B, Bezanilla F. 2002. Tracking voltage-dependent conformational changes in skeletal muscle sodium channel during activation. The Journal of General Physiology 120:629-645. doi:10.1085/jgp.20028679
10. Chen C, Calhoun JD, Zhang Y, Lopez-Santiago L, Zhou N, Davis TH, Salzer JL, Isom LL. 2012. Identification of the cysteine residue responsible for disulfide linkage of Na+ channel alpha and beta2 subunits. Journal of Biological Chemistry 287:39061-39069. doi:10.1074/jbc.M112.397646
11. Chen C, Cannon SC. 1995. Modulation of Na+channel inactivation by the beta 1 subunit: a deletion analysis. PfluGers Archiv European Journal of Physiology 431:186-195. doi:10.1007/BF00410190
12. Claes LR, Deprez L, Suls A, Baets J, Smets K, Van Dyck T, Deconinck T, Jordanova A, De Jonghe P. 2009. The SCN1A variant database: a novel research and diagnostic tool. Human Mutation 30:E904-920. doi:10.1002/humu.21083
13. Copits BA, Swanson GT. 2012. Dancing partners at the synapse: auxiliary subunits that shape kainate receptor function. Nature Reviews Neuroscience 13:675-686. doi:10.1038/nrn3335
14. Deschênes I, Armoundas AA, Jones SP, Tomaselli GF. 2008. Post-transcriptional gene silencing of KChIP2 and Navb1 in neonatal rat cardiac myocytes reveals a functional association between na and ito currents. Journal of Molecular and Cellular Cardiology 45:336-346. doi:10.1016/j.yjmcc.2008.05.001
15. Doeser A, Soares-da-Silva P, Beck H, Uebachs M. 2014. The effects of eslicarbazepine on persistent Na+ current and the role of the Na+ channel beta subunits. Epilepsy Research 108:202-211. doi:10.1016/j.eplepsyres.2013.11.022
16. Dolphin AC. 2012. Calcium channel auxiliary alpha2delta and beta subunits: trafficking and one step beyond. Nature Reviews. Neuroscience 13:542-555. doi:10.1038/nrn3311
17. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of coot. Acta Crystallographica Section D Biological Crystallography 66:486-501. doi:10.1107/S0907444910007493
18. Gajewiak J, Azam L, Imperial J, Walewska A, Green BR, Bandyopadhyay PK, Raghuraman S, Ueberheide B, Bern M, Zhou HM, Minassian NA, Hagan RH, Flinspach M, Liu Y, Bulaj G, Wickenden AD, Olivera BM, Yoshikami D, Zhang M-M. 2014. A disulfide tether stabilizes the block of sodium channels by the conotoxin muO section sign-GVIIJ. Proceedings of the National Academy of Sciences of the United States of America 111:2758-2763. doi:10.1073/pnas.1324189111
19. Gee NS, Brown JP, Dissanayake VUK, Offord J, Thurlow R, Woodruff GN. 1996. The novel anticonvulsant drug, gabapentin (neurontin), binds to the subunit of a calcium channel. Journal of Biological Chemistry 271:5768-5776. doi:10.1074/jbc.271.10.5768
20. Gersbacher MT, Kim DY, Bhattacharyya R, Kovacs DM. 2010. Identification of BACE1 cleavage sites in human voltage-gated sodium channel beta 2 subunit. Molecular Neurodegeneration 5. doi:10.1186/1750-1326-5-61
21. Gilchrist J, Das S, Van Petegem F, Bosmans F 2013. Crystallographic insights into sodium-channel modulation by the beta4 subunit. Proceedings of the National Academy of Sciences of the United states of America 110: E5016-E5024. doi:10.1073/pnas.1314557110
22. Gilchrist J, Olivera BM, Bosmans F. 2014. Animal toxins influence voltage-gated sodium channel function. Handbook of Experimental Pharmacology 221: 203-229. doi:10.1007/978-3-642-41588-3_10
23. Hille B. 2001. Ion Channels of Excitable Membranes, 814. Sinauer Associates, Inc., MA, USA.
24. Horn R, Ding S, Gruber HJ. 2000. Immobilizing the moving parts of voltage-gated ion channels. The Journal of General Physiology 116:461-476. doi:10.1085/jgp.116.3.461
25. Isom L, De Jongh K, Patton D, Reber B, Offord J, Charbonneau H, Walsh K, Goldin A, Catterall W. 1992. Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 256:839-842. doi:10.1126/science.1375395
26. Isom LL, Ragsdale DS, De Jongh KS, Westenbroek RE, Reber BFX, Scheuer T, Catterall WA. 1995. Structure and function of the beta2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83:433-442. doi:10.1016/0092-8674(95)90121-3
27. Isom LL, Scheuer T, Brownstein AB, Ragsdale DS, Murphy BJ, Catterall WA. 1995b. Functional co-expression of the beta 1 and type IIA alpha subunits of sodium channels in a mammalian cell line. Journal of Biological Chemistry 270:3306-3312.
28. Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R. 2003. X-ray structure of a voltage-dependent k+ channel. Nature 423:33-41. doi:10.1038/nature01580
29. Johnson D, Bennett ES. 2006. Isoform-specific effects of the beta2 subunit on voltage-gated sodium channel gating. Journal of Biological Chemistry 281:25875-25881. doi:10.1074/jbc.M605060200
30. Kabsch W. 2010. XDS. Acta Crystallographica Section D Biological Crystallography 66:125-132. doi:10.1107/S0907444909047337
31. Kim DY, Ingano LAM, Carey BW, Pettingell WH, Kovacs DM. 2005. Presenilin/gamma secretase-mediated cleavage of the voltage-gated sodium channel beta2-subunit regulates cell adhesion and migration. Journal of Biological Chemistry 280:23251-23261. doi:10.1074/jbc.M412938200
32. Langer G, Cohen SX, Lamzin VS, Perrakis A. 2008. Automated macromolecular model building for x-ray crystallography using ARP/wARP version 7. Nature Protocols 3:1171-1179. doi:10.1038/nprot.2008.91
33. Li RG, Wang Q, Xu YJ, Zhang M, Qu XK, Liu X, Fang WY, Yang YQ. 2013. Mutations of the SCN4B-encoded sodium channel beta4 subunit in familial atrial fibrillation. International Journal of Molecular Medicine 32:144-150. doi:10.3892/ijmm.2013.1355
34. Long SB, Tao X, Campbell EB, MacKinnon R. 2007. Atomic structure of a voltage-dependent k+ channel in a lipid membrane-like environment. Nature 450:376-382. doi:10.1038/nature06265
35. Lopez-Santiago LF, Pertin M, Morisod X, Chen C, Hong S, Wiley J, Decosterd I, Isom LL. 2006. Sodium channel beta2 subunits regulate tetrodotoxin-sensitive sodium channels in small dorsal root ganglion neurons and modulate the response to pain. Journal of Neuroscience 26:7984-7994. doi:10.1523/JNEUROSCI.2211-06.2006
36. Maier SK, Westenbroek RE, McCormick KA, Curtis R, Scheuer T, Catterall WA. 2004. Distinct subcellular localization of different sodium channel alpha and beta subunits in single ventricular myocytes from mouse heart. Circulation 109:1421-1427. doi:10.1161/01.CIR.0000121421.61896.24
37. Makita N, Bennett PB, George AL. 1996. Molecular determinants of beta 1 subunit-induced gating modulation in voltage-dependent Na+ channels. Journal of Neuroscience 16:7117-7127.
38. Malhotra JD, Chen C, Rivolta I, Abriel H, Malhotra R, Mattei LN, Brosius FC, Kass RS, Isom LL. 2001. Characterization of sodium channel alpha-and beta-subunits in rat and mouse cardiac myocytes. Circulation 103:1303-1310. doi:10.1161/01.CIR.103.9.1303
39. Marionneau C, Carrasquillo Y, Norris AJ, Townsend RR, Isom LL, Link AJ, Nerbonne JM. 2012. The sodium channel accessory subunit nav 1 regulates neuronal excitability through modulation of repolarizing voltage-gated k+ channels. Journal of Neuroscience 32:5716-5727. doi:10.1523/JNEUROSCI.6450-11.2012
40. Martin MF, Rochat H, Marchot P, Bougis PE. 1987. Use of high performance liquid chromatography to demonstrate quantitative variation in components of venom from the scorpion androctonus australis hector. Toxicon 25:569-573. doi:10.1016/0041-0101(87)90293-5
41. McCormick KA, Isom LL, Ragsdale D, Smith D, Scheuer T, Catterall WA. 1998. Molecular determinants of Na+ channel function in the extracellular domain of the beta 1 subunit. Journal of Biological Chemistry 273:3954-3962. doi:10.1074/jbc.273.7.3954
42. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. Journal of Applied Crystallography 40:658-674. doi:10.1107/S0021889807021206
43. Medeiros-Domingo A, Kaku T, Tester DJ, Iturralde-Torres P, Itty A, Ye B, Valdivia C, Ueda K, Canizales-Quinteros S, Tusié-Luna MT, Makielski JC, Ackerman MJ. 2007. SCN4B-encoded sodium channel beta4 subunit in congenital long-QT syndrome. Circulation 116:134-142. doi:10.1161/CIRCULATIONAHA.106.659086
44. Middleton RE, Warren VA, Kraus RL, Hwang JC, Liu CJ, Dai G, Brochu RM, Kohler MG, Gao Y-D, Garsky VM, Bogusky MJ, Mehl JT, Cohen CJ, Smith MM. 2002. Two tarantula peptides inhibit activation of multiple sodium channels. Biochemistry 41:14734-14747. doi:10.1021/bi026546a
45. Milstein AD, Nicoll RA. 2008. Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends in Pharmacological Sciences 29:333-339. doi:10.1016/j.tips.2008.04.004
46. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M. 2006. HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallographica Section D Biological Crystallography 62:859-866. doi:10.1107/S0907444906019949
47. Morgan K, Stevens EB, Shah B, Cox PJ, Dixon AK, Lee K, Pinnock RD, Hughes J, Richardson PJ, Mizuguchi K, Jackson AP. 2000. Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proceedings of the National Academy of Sciences of the United States of America 97:2308-2313. doi:10.1073/pnas.030362197
48. Namadurai S, Balasuriya D, Rajappa R, Wiemhofer M, Stott K, Klingauf J, Edwardson JM, Chirgadze DY, Jackson AP. 2014. Crystal structure and molecular imaging of the Nav channel beta3 subunit indicates a trimeric assembly. Journal of Biological Chemistry 289:10797-10811. doi:10.1074/jbc.M113.527994
49. Namadurai S, Yereddi NR, Cusdin FS, Huang CL, Chirgadze DY, Jackson AP. 2015. A new look at sodium channel b subunits. Open Biology 5. doi:10.1098/rsob.140192
50. Nguyen HM, Miyazaki H, Hoshi N, Smith BJ, Nukina N, Goldin AL, Chandy KG. 2012. Modulation of voltage-gated k+ channels by the sodium channel beta1 subunit. Proceedings of the National Academy of Sciences of the United States of the America 109:18577-18582. doi:10.1073/pnas.1209142109
51. + channel beta2 subunits is neuroprotective in a mouse model of multiple sclerosis. Molecular and Cellular Neuroscience 40:143-155. doi:10.1016/j.mcn.2008.10.001
52. + channel beta1B: a secreted cell adhesion molecule involved in human epilepsy. Journal of Neuroscience 31:14577-14591. doi:10.1523/JNEUROSCI.0361-11.2011
53. Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA. 2012. Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486:135-139. doi:10.1038/nature11077
54. Payandeh J, Scheuer T, Zheng N, Catterall WA. 2011. The crystal structure of a voltage-gated sodium channel. Nature 475:353-358. doi:10.1038/nature10238
55. Qu Y, Rogers JC, Chen S-F, McCormick KA, Scheuer T, Catterall WA. 1999. Functional roles of the extracellular segments of the sodium channel alpha subunit in voltage-dependent gating and modulation by beta1 subunits. Journal of Biological Chemistry 274:32647-32654. doi:10.1074/jbc.274.46.32647
56. Shaya D, Findeisen F, Abderemane-Ali F, Arrigoni C, Wong S, Nurva SR, Loussouarn G, Minor DL. 2014. Structure of a prokaryotic sodium channel pore reveals essential gating elements and an outer ion binding site common to eukaryotic channels. Journal of Molecular Biology 426:467-483. doi:10.1016/j.jmb.2013.10.010
57. Sheets MF, Kyle JW, Kallen RG, Hanck DA. 1999. The na channel voltage sensor associated with inactivation is localized to the external charged residues of domain IV, S4. Biophysical Journal 77:747-757. doi:10.1016/S0006-3495(99)76929-8
58. Tan B-H, Pundi KN, Van Norstrand DW, Valdivia CR, Tester DJ, Medeiros-Domingo A, Makielski JC, Ackerman MJ. 2010. Sudden infant death syndrome-associated mutations in the sodium channel beta subunits. Heart Rhythm 7:771-778. doi:10.1016/j.hrthm.2010.01.032
59. Van Petegem F, Clark KA, Chatelain FC, Minor DL. 2004. Structure of a complex between a voltage-gated calcium channel beta-subunit and an alpha-subunit domain. Nature 429:671-675. doi:10.1038/nature02588
60. Watanabe H, Darbar D, Kaiser DW, Jiramongkolchai K, Chopra S, Donahue BS, Kannankeril PJ, Roden DM. 2009. Mutations in sodium channel beta1-and beta2-subunits associated with atrial fibrillation. Circulation: Arrhythmia and Electrophysiology 2:268-275. doi:10.1161/CIRCEP.108.779181
61. Wilson MJ, Zhang M-M, Azam L, Olivera BM, Bulaj G, Yoshikami D. 2011. Navbeta subunits modulate the inhibition of NaV1.8 by the analgesic gating modifier muO-conotoxin MrVIB. Journal of Pharmacology and Experimental Therapeutics 338:687-693. doi:10.1124/jpet.110.178343
62. Wilson MJ, Zhang M-M, Gajewiak J, Azam L, Rivier JE, Olivera BM, Yoshikami D. 2015. Alpha-and beta-subunit composition of voltage-gated sodium channels investigated with mu-conotoxins and the recently discovered muO-conotoxin GVIIJ. Journal of Neurophysiology 113:2289-2301. doi:10.1152/jn.01004.2014
63. Yu FH, Westenbroek RE, Silos-Santiago I, McCormick KA, Lawson D, Ge P, Ferriera H, Lilly J, DiStefano PS, Catterall WA, Scheuer T, Curtis R. 2003. Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2. The Journal of Neuroscience 23:7577-7585.
64. Yu Y, Ulbrich MH, Li Ming-hui, Dobbins S, Zhang WK, Tong L, Isacoff EY, Yang J. 2012. Molecular mechanism of the assembly of an acid-sensing receptor ion channel complex. Nature Communications 3:1252. doi:10.1038/ncomms2257
65. Zhang MM, Gajewiak J, Azam L, Bulaj G, Olivera BM, Yoshikami D. 2015. Probing the redox states of sodium channel cysteines at the binding site of muO-conotoxin GVIIJ. Biochemistry 54:3911-3920. doi:10.1021/acs.biochem.5b00390
66. Zhang MM, Wilson MJ, Azam L, Gajewiak J, Rivier JE, Bulaj G, Olivera BM, Yoshikami D. 2013. Co-expression of Navbeta subunits alters the kinetics of inhibition of voltage-gated sodium channels by pore-blocking muconotoxins. British Journal of Pharmacology 168:1597-1610. doi:10.1111/bph.12051
67. Zhang X, Ren W, DeCaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, He J, Wang J, Clapham DE, Yan N. 2012. Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:130-134. doi:10.1038/nature11054
68. Zimmer T, Benndorf K. 2002. The human heart and rat brain IIA na+ channels interact with different molecular regions of the beta1 subunit. The Journal of General Physiology 120:887-895. doi:10.1085/jgp.20028703
69. Zimmer T, Benndorf K. 2007. The intracellular domain of the beta2 subunit modulates the gating of cardiac Nav1.5 channels. Biophysical Journal 92:3885-3892. doi:10.1529/biophysj.106.098889
70. Zimmer T, Biskup C, Bollensdorff C, Benndorf K. 2002. The beta1 subunit but not the beta2 subunit colocalizes with the human heart Na+ channel (hH1) already within the endoplasmic reticulum. The Journal of Membrane Biology 186:13-21. doi:10.1007/s00232-001-0131-0