Alternative splicing of the cardiac sodium channel creates multiple variants of mutant T1620K channels

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Walzik, Stefan ^a   Schroeter, Annett ^a   Benndorf, Klaus ^a   Zimmer, Thomas ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; SODIUM CHANNEL NAV1.5; SODIUM CHANNEL NAV1.5A; SODIUM CHANNEL NAV1.5C; SODIUM CHANNEL NAV1.5D; SODIUM CHANNEL NAV1.5E; UNCLASSIFIED DRUG; ISOPROTEIN; SODIUM CHANNEL; SODIUM CHANNEL PROTEIN TYPE 5 SUBUNIT ALPHA;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL STRAIN HEK293; CONTROLLED STUDY; EXON; GAIN OF FUNCTION MUTATION; GENE MUTATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; LOSS OF FUNCTION MUTATION; MEMBRANE CURRENT; MEMBRANE ELECTROPHYSIOLOGY; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN VARIANT; STEADY STATE; ELECTROPHYSIOLOGY; GENETICS; METABOLISM;

MAMMALIA;

ALTERNATIVE SPLICING; ELECTROPHYSIOLOGICAL PROCESSES; HEK293 CELLS; HUMANS; MUTANT PROTEINS; MUTATION; PROTEIN ISOFORMS; SODIUM CHANNELS;

EID: 79955731749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019188     Document Type: Article

References (43)

1. Catterall WA, (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26: 13-25.
2. Blechschmidt S, Haufe V, Benndorf K, Zimmer T, (2008) Voltage-gated Na+ channel transcript patterns in the mammalian heart are species-dependent. Prog Biophys Mol Biol 98: 309-318.
3. Catterall WA, Goldin AL, Waxman SG, (2005) International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57: 397-409.
4. Gui J, Wang T, Jones RP, Trump D, Zimmer T, et al. (2010) Multiple loss-of-function mechanisms contribute to SCN5A-related familial sick sinus syndrome. PLoS One 5: e10985.
5. Zimmer T, Surber R, (2008) SCN5A channelopathies-an update on mutations and mechanisms. Prog Biophys Mol Biol 98: 120-136.
6. Makita N, Sasaki K, Groenewegen WA, Yokota T, Yokoshiki H, et al. (2005) Congenital atrial standstill associated with coinheritance of a novel SCN5A mutation and connexin 40 polymorphisms. Heart Rhythm 2: 1128-1134.
7. Ruan Y, Liu N, Bloise R, Napolitano C, Priori SG, (2007) Gating properties of SCN5A mutations and the response to mexiletine in long-QT syndrome type 3 patients. Circulation 116: 1137-1144.
8. Wehrens XH, Abriel H, Cabo C, Benhorin J, Kass RS, (2000) Arrhythmogenic mechanism of an LQT-3 mutation of the human heart Na(+) channel alpha-subunit: A computational analysis. Circulation 102: 584-590.
9. 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.
10. Kyndt F, Probst V, Potet F, Demolombe S, Chevallier JC, et al. (2001) Novel SCN5A mutation leading either to isolated cardiac conduction defect or Brugada syndrome in a large French family. Circulation 104: 3081-3086.
11. Smits JP, Koopmann TT, Wilders R, Veldkamp MW, Opthof T, et al. (2005) A mutation in the human cardiac sodium channel (E161K) contributes to sick sinus syndrome, conduction disease and Brugada syndrome in two families. J Mol Cell Cardiol 38: 969-981.
12. Zhang Y, Wang T, Ma A, Zhou X, Gui J, et al. (2008) Correlations between clinical and physiological consequences of the novel mutation R878C in a highly conserved pore residue in the cardiac Na+ channel. Acta Physiol (Oxf) 194: 311-323.
13. Grant AO, Carboni MP, Neplioueva V, Starmer CF, Memmi M, et al. (2002) Long QT syndrome, Brugada syndrome, and conduction system disease are linked to a single sodium channel mutation. J Clin Invest 110: 1201-1209.
14. Laitinen-Forsblom PJ, Makynen P, Makynen H, Yli-Mayry S, Virtanen V, et al. (2006) SCN5A mutation associated with cardiac conduction defect and atrial arrhythmias. J Cardiovasc Electrophysiol 17: 480-485.
15. 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.
16. Olson TM, Michels VV, Ballew JD, Reyna SP, Karst ML, et al. (2005) Sodium channel mutations and susceptibility to heart failure and atrial fibrillation. JAMA 293: 447-454.
17. Abriel H, (2010) Cardiac sodium channel Na(v)1.5 and interacting proteins: Physiology and pathophysiology. J Mol Cell Cardiol 48: 2-11.
18. Gui J, Wang T, Trump D, Zimmer T, Lei M, (2010) Mutation-specific effects of polymorphism H558R in SCN5A-related sick sinus syndrome. J Cardiovasc Electrophysiol 21: 564-573.
19. Tan BH, Valdivia CR, Rok BA, Ye B, Ruwaldt KM, et al. (2005) Common human SCN5A polymorphisms have altered electrophysiology when expressed in Q1077 splice variants. Heart Rhythm 2: 741-747.
20. Wang DW, Desai RR, Crotti L, Arnestad M, Insolia R, et al. (2007) Cardiac sodium channel dysfunction in sudden infant death syndrome. Circulation 115: 368-376.
21. Keller DI, Rougier JS, Kucera JP, Benammar N, Fressart V, et al. (2005) Brugada syndrome and fever: genetic and molecular characterization of patients carrying SCN5A mutations. Cardiovasc Res 67: 510-519.
22. Kranjcec D, Bergovec M, Rougier JS, Raguz M, Pavlovic S, et al. (2007) Brugada syndrome unmasked by accidental inhalation of gasoline vapors. Pacing Clin Electrophysiol 30: 1294-1298.
23. Yang P, Kanki H, Drolet B, Yang T, Wei J, et al. (2002) Allelic variants in long-QT disease genes in patients with drug-associated torsades de pointes. Circulation 105: 1943-1948.
24. Tateyama M, Kurokawa J, Terrenoire C, Rivolta I, Kass RS, (2003) Stimulation of protein kinase C inhibits bursting in disease-linked mutant human cardiac sodium channels. Circulation 107: 3216-3222.
25. Tateyama M, Rivolta I, Clancy CE, Kass RS, (2003) Modulation of cardiac sodium channel gating by protein kinase A can be altered by disease-linked mutation. J Biol Chem 278: 46718-46726.
26. Leoni AL, Gavillet B, Rougier JS, Marionneau C, Probst V, et al. (2010) Variable Na(v)1.5 protein expression from the wild-type allele correlates with the penetrance of cardiac conduction disease in the Scn5a(+/-) mouse model. PLoS One 5: e9298.
27. Shang LL, Dudley SC Jr, (2005) Tandem promoters and developmentally regulated 5′- and 3′-mRNA untranslated regions of the mouse Scn5a cardiac sodium channel. J Biol Chem 280: 933-940.
28. Schroeter A, Walzik S, Blechschmidt S, Haufe V, Benndorf K, et al. (2010) Structure and function of splice variants of the cardiac voltage-gated sodium channel Na(v)1.5. J Mol Cell Cardiol 49: 16-24.
29. 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.
30. 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 U S A 89: 554-558.
31. Makielski JC, Ye B, Valdivia CR, Pagel MD, Pu J, et al. (2003) A ubiquitous splice variant and a common polymorphism affect heterologous expression of recombinant human SCN5A heart sodium channels. Circ Res 93: 821-828.
32. Fraser SP, Diss JK, Chioni AM, Mycielska ME, Pan H, et al. (2005) Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin Cancer Res 11: 5381-5389.
33. Ou SW, Kameyama A, Hao LY, Horiuchi M, Minobe E, et al. (2005) Tetrodotoxin-resistant Na+ channels in human neuroblastoma cells are encoded by new variants of Nav1.5/SCN5A. Eur J Neurosci 22: 793-801.
34. Camacho JA, Hensellek S, Rougier JS, Blechschmidt S, Abriel H, et al. (2006) Modulation of Nav1.5 channel function by an alternatively spliced sequence in the DII/DIII linker region. J Biol Chem 281: 9498-9506.
35. Zimmer T, Bollensdorff C, Haufe V, Birch-Hirschfeld E, Benndorf K, (2002) Mouse heart Na+ channels: primary structure and function of two isoforms and alternatively spliced variants. Am J Physiol Heart Circ Physiol 282: H1007-1017.
36. 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. J Membr Biol 186: 13-21.
37. Chioni AM, Fraser SP, Pani F, Foran P, Wilkin GP, et al. (2005) A novel polyclonal antibody specific for the Na(v)1.5 voltage-gated Na(+) channel 'neonatal' splice form. J Neurosci Methods 147: 88-98.
38. Cocquet J, Chong A, Zhang G, Veitia RA, (2006) Reverse transcriptase template switching and false alternative transcripts. Genomics 88: 127-131.
39. Roy SW, Irimia M, (2008) When good transcripts go bad: artifactual RT-PCR 'splicing' and genome analysis. Bioessays 30: 601-605.
40. Clancy CE, Tateyama M, Liu H, Wehrens XH, Kass RS, (2003) Non-equilibrium gating in cardiac Na+ channels: an original mechanism of arrhythmia. Circulation 107: 2233-2237.
41. Brackenbury WJ, Chioni AM, Diss JK, Djamgoz MB, (2007) The neonatal splice variant of Nav1.5 potentiates in vitro invasive behaviour of MDA-MB-231 human breast cancer cells. Breast Cancer Res Treat 101: 149-160.
42. Chioni AM, Brackenbury WJ, Calhoun JD, Isom LL, Djamgoz MB, (2009) A novel adhesion molecule in human breast cancer cells: voltage-gated Na+ channel beta1 subunit. Int J Biochem Cell Biol 41: 1216-1227.
43. Onkal R, Mattis JH, Fraser SP, Diss JK, Shao D, et al. (2008) Alternative splicing of Nav1.5: an electrophysiological comparison of 'neonatal' and 'adult' isoforms and critical involvement of a lysine residue. J Cell Physiol 216: 716-726.