A proton leak current through the cardiac sodium channel is linked to mixed arrhythmia and the dilated cardiomyopathy phenotype

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Gosselin Badaroudine, Pascal ^a   Keller, Dagmar I ^b,c   Huang, Hai ^a   Pouliot, Valérie ^a   Chatelier, Aurélien ^a,d   Osswald, Stefan ^c   Brink, Marijke ^c   Chahine, Mohamed ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d UNIVERSITÉ DE POITIERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HISTIDINE; PROTON; SODIUM CHANNEL NAV1.5; SODIUM CHANNEL; SODIUM CHANNEL PROTEIN TYPE 5 SUBUNIT ALPHA;

ACIDIFICATION; ADULT; ARTICLE; BIOPHYSICS; CASE REPORT; CELL PH; CONGESTIVE CARDIOMYOPATHY; DISEASE ASSOCIATION; DOWNSTREAM PROCESSING; FAMILY HISTORY; GENE; GENE LOCATION; GENETIC CONSERVATION; GENETIC SCREENING; HEART ARRHYTHMIA; HEART ATRIUM FLUTTER; HEART MUSCLE CONDUCTION DISTURBANCE; HEART VENTRICLE TACHYCARDIA; HETEROLOGOUS EXPRESSION; HUMAN; MALE; MUTATIONAL ANALYSIS; NUCLEOTIDE SEQUENCE; PH ELECTRODE; PHENOTYPE; PROTEIN DOMAIN; PROTEIN FAMILY; SCN5A GENE; WILD TYPE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; CELL LINE; GENETICS; HEART MUSCLE CELL; METABOLISM; MOLECULAR GENETICS; MUTATION; OOCYTE; PATHOPHYSIOLOGY; PEDIGREE; PH; XENOPUS;

ADULT; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ARRHYTHMIAS, CARDIAC; BASE SEQUENCE; CARDIOMYOPATHY, DILATED; CELL LINE; HUMANS; HYDROGEN-ION CONCENTRATION; MALE; MOLECULAR SEQUENCE DATA; MUTATION; MYOCYTES, CARDIAC; OOCYTES; PEDIGREE; PHENOTYPE; PROTONS; SODIUM CHANNELS; XENOPUS;

EID: 84861664954     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038331     Document Type: Article

References (46)

1. Gellens ME, George AL Jr, Chen LQ, Chahine M, Horn R, et al. (1992) Primary structure and functional expression of the human cardiac tetrodotoxin-insensitive voltage-dependent sodium channel. Proc Natl Acad Sci USA 89: 554-558.
2. Splawski I, Shen J, Timothy KW, Lehmann MH, Priori S, et al. (2000) Spectrum of mutations in long-QT syndrome genes. KVLQT1, HERG, SCN5A, KCNE1, and KCNE2. Circulation 102: 1178-1185.
3. Brugada P, Brugada J, (1992) Right bundle branch block, persistent ST segment elevation and sudden cardiac death: a distinct clinical and electrocardiographic syndrome. J Am Coll Cardiol 20: 1391-1396.
4. Chen Q, Kirsch GE, Zhang D, Brugada R, Brugada J, et al. (1998) Genetic basis and molecular mechanism for idiopathic ventricular fibrillation. Nature 392: 293-296.
5. George AL Jr, (2005) Inherited disorders of voltage-gated sodium channels. J Clin Invest 115: 1990-1999.
6. Wang Q, Shen J, Splawski I, Atkinson D, Li Z, et al. (1995) SCN5A mutations associated with an inherited cardiac arrhythmia, long QT syndrome. Cell 80: 805-811.
7. Antzelevitch C, (2006) Brugada syndrome. Pacing Clin Electrophysiol 29: 1130-1159.
8. Li Q, Huang H, Liu G, Lam K, Rutberg J, et al. (2009) Gain-of-function mutation of Nav1.5 in atrial fibrillation enhances cellular excitability and lowers the threshold for action potential firing. Biochem Biophys Res Commun 380: 132-137.
9. Vatta M, Dumaine R, Varghese G, Richard TA, Shimizu W, et al. (2002) Genetic and biophysical basis of sudden unexplained nocturnal death syndrome (SUNDS), a disease allelic to Brugada syndrome. Hum Mol Genet 11: 337-345.
10. Tan BH, Iturralde-Torres P, Medeiros-Domingo A, Nava S, Tester DJ, et al. (2007) A novel C-terminal truncation SCN5A mutation from a patient with sick sinus syndrome, conduction disorder and ventricular tachycardia. Cardiovasc Res 76: 409-417.
11. Surber R, Hensellek S, Prochnau D, Werner GS, Benndorf K, et al. (2008) Combination of cardiac conduction disease and long QT syndrome caused by mutation T1620K in the cardiac sodium channel. Cardiovasc Res 77: 740-748.
12. Michels VV, Moll PP, Miller FA, Tajik AJ, Chu JS, et al. (1992) The frequency of familial dilated cardiomyopathy in a series of patients with idiopathic dilated cardiomyopathy. N Engl J Med 326: 77-82.
13. Keeling PJ, Gang Y, Smith G, Seo H, Bent SE, et al. (1995) Familial dilated cardiomyopathy in the United Kingdom. Br Heart J 73: 417-421.
14. Olson TM, Keating MT, (1996) Mapping a cardiomyopathy locus to chromosome 3p22-p25. J Clin Invest 97: 528-532.
15. Olson TM, Michels VV, Ballew JD, Reyna SP, Karst ML, et al. (2005) Sodium channel mutations and susceptibility to heart failure and atrial fibrillation. J Am Med Assoc 293: 447-454.
16. Shi R, Zhang Y, Yang C, Huang C, Zhou X, et al. (2008) The cardiac sodium channel mutation delQKP 1507-1509 is associated with the expanding phenotypic spectrum of LQT3, conduction disorder, dilated cardiomyopathy, and high incidence of youth sudden death. Europace 10: 1329-1335.
17. Benson DW, Wang DW, Dyment M, Knilans TK, Fish FA, et al. (2003) Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest 112: 1019-1028.
18. Bezzina CR, Rook MB, Groenewegen WA, Herfst LJ, van der Wal AC, et al. (2003) Compound heterozygosity for mutations (W156X and R225W) in SCN5A associated with severe cardiac conduction disturbances and degenerative changes in the conduction system. Circ Res 92: 159-168.
19. Ge J, Sun A, Paajanen V, Wang S, Su C, et al. (2008) Molecular and clinical characterization of a novel SCN5A mutation associated with atrioventricular block and dilated cardiomyopathy. Circ Arrhythm Electrophysiol 1: 83-92.
20. McNair WP, Ku L, Taylor MR, Fain PR, Dao D, et al. (2004) SCN5A mutation associated with dilated cardiomyopathy, conduction disorder, and arrhythmia. Circulation 110: 2163-2167.
21. Nguyen TP, Wang DW, Rhodes TH, George AL Jr, (2008) Divergent biophysical defects caused by mutant sodium channels in dilated cardiomyopathy with arrhythmia. Circ Res 102: 364-371.
22. McNair WP, Sinagra G, Taylor MR, Di LA, Ferguson DA, et al. (2011) SCN5A Mutations Associate With Arrhythmic Dilated Cardiomyopathy and Commonly Localize to the Voltage-Sensing Mechanism. J Am Coll Cardiol 57: 2160-2168.
23. Cheng J, Morales A, Siegfried JD, Li D, Norton N, et al. (2010) SCN5A rare variants in familial dilated cardiomyopathy decrease peak sodium current depending on the common polymorphism H558R and common splice variant Q1077del. Clin Transl Sci 3: 287-294.
24. Wang Q, Li Z, Shen J, Keating MT, (1996) Genomic organization of the human SCN5A gene encoding the cardiac sodium channel. Genomics 34: 9-16.
25. Bergeron MJ, Gagnon E, Caron L, Isenring P, (2006) Identification of key functional domains in the C terminus of the K+-Cl- cotransporters. J Biol Chem 281: 15959-15969.
26. Chahine M, Chen LQ, Barchi RL, Kallen RG, Horn R, (1992) Lidocaine block of human heart sodium channels expressed in Xenopus oocytes. J Mol Cell Cardiol 24: 1231-1236.
27. 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: 78-82.
28. Groenewegen WA, Firouzi M, Bezzina CR, Vliex S, van Langen IM, et al. (2003) A cardiac sodium channel mutation cosegregates with a rare connexin40 genotype in familial atrial standstill. Circ Res 92: 14-22.
29. Starace DM, Bezanilla F, (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427: 548-553.
30. Sokolov S, Scheuer T, Catterall WA, (2007) Gating pore current in an inherited ion channelopathy. Nature 446: 76-78.
31. Gunthorpe MJ, Smith GD, Davis JB, Randall AD, (2001) Characterisation of a human acid-sensing ion channel (hASIC1a) endogenously expressed in HEK293 cells. Pflugers Arch 442: 668-674.
32. Schonberger J, Seidman CE, (2001) Many roads lead to a broken heart: the genetics of dilated cardiomyopathy. Am J Hum Genet 69: 249-260.
33. Seidman JG, Seidman C, (2001) The genetic basis for cardiomyopathy: from mutation identification to mechanistic paradigms. Cell 104: 557-567.
34. Makita N, Yamamoto H, Sasaki K, Yokoshiki H, Motomura H, et al. (2006) Genetic Factors Conferring Congenital Sick Sinus Syndrome in SCN5A Mutation Carriers. Circulation 114: II505.
35. Struyk AF, Cannon SC, (2007) A Na+ channel mutation linked to hypokalemic periodic paralysis exposes a proton-selective gating pore. J Gen Physiol 130: 11-20.
36. Pomès R, Roux B, (2002) Molecular mechanism of H+ conduction in the single-file water chain of the gramicidin channel. Biophys J 82: 2304-2316.
37. Yang NB, Horn R, (1995) Evidence for voltage-dependent S4 movement in sodium channels. Neuron 15: 213-218.
38. Yang N, George AL Jr, Horn R, (1996) Molecular basis of charge movement in voltage-gated sodium channels. Neuron 16: 113-122.
39. Piwnica-Worms D, Jacob R, Horres CR, Lieberman M, (1985) Na/H exchange in cultured chick heart cells. pHi regulation. J Gen Physiol 85: 43-64.
40. Chahine M, Bkaily G, Nader M, Al-Khoury J, Jacques D, et al. (2005) NHE-1-dependent intracellular sodium overload in hypertrophic hereditary cardiomyopathy: prevention by NHE-1 inhibitor. J Mol Cell Cardiol 38: 571-582.
41. Kohmoto O, Spitzer KW, Movsesian MA, Barry WH, (1990) Effects of intracellular acidosis on [Ca2+]i transients, transsarcolemmal Ca2+ fluxes, and contraction in ventricular myocytes. Circ Res 66: 622-632.
42. Fabiato A, Fabiato F, (1978) Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol 276: 233-255.
43. Stergiopoulos K, Alvarado JL, Mastroianni M, Ek-Vitorin JF, Taffet SM, et al. (1999) Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ Res 84: 1144-1155.
44. Duffy HS, Ashton AW, O'Donnell P, Coombs W, Taffet SM, et al. (2004) Regulation of connexin43 protein complexes by intracellular acidification. Circ Res 94: 215-222.
45. Bukauskas FF, Bukauskiene A, Bennett MVL, Verselis VK, (2001) Gating properties of gap junction channels assembled from connexin43 and connexin43 fused with green fluorescent protein. Biophys J 81: 137-152.
46. Chahine M, Sirois J, Marcotte P, Chen LQ, 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 μ- conotoxin GIIIA binding site. Biophys J 75: 236-246.