Sodium channels as macromolecular complexes: Implications for inherited arrhythmia syndromes

Cardiovascular Research

Volumn 67, Issue 3, 2005, Pages 448-458

  Meadows, L S ^a   Isom, L L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Auxilliary subunits; Cardiac myocytes; Cell adhesion molecules; Channel physiology; Sodium channel

Indexed keywords

ANKYRIN; ION CHANNEL; PHOSPHATASE; PHOSPHOTRANSFERASE; PROTEIN; SCLEROPROTEIN; SODIUM; SODIUM CHANNEL; SYNTROPHIN; VOLTAGE GATED SODIUM CHANNEL;

BRAIN; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CYTOSKELETON; GENE; GENETIC DISORDER; HEART; HEART ARRHYTHMIA; HUMAN; IN VIVO STUDY; MACROMOLECULE; MOLECULAR INTERACTION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; SYNDROME;

ANIMALS; ANKYRINS; ANTI-ARRHYTHMIA AGENTS; ARRHYTHMIA; DYSTROPHIN-ASSOCIATED PROTEINS; HUMANS; ION CHANNEL GATING; LONG QT SYNDROME; MACROMOLECULAR SUBSTANCES; MYOCYTES, CARDIAC; NERVE GROWTH FACTORS; PROTEIN TRANSPORT; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 22544486622     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2005.04.003     Document Type: Review

References (125)

1. D.M. Roden, J.R. Balser, A.L. George Jr., and M.E. Anderson Cardiac ion channels Annu Rev Physiol 64 2002 431 475
2. W.A. Catterall From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels Neuron 26 2000 13 25
3. S. Poliak, and E. Peles The local differentiation of myelinated axons at nodes of Ranvier Nat Rev Neurosci 4 2003 968 980
4. J.S. Trimmer, and K.J. Rhodes Localization of voltage-gated ion channels in mammalian brain Annu Rev Physiol 66 2004 477 519
5. B.K. Krueger, and M.P. Blaustein Sodium channels in presynaptic nerve terminals J Gen Physiol 76 1980 287 313
6. R. Lipowsky, T. Gillessen, and C. Alzheimer Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells J Neurophysiol 76 1996 2181 2191
7. J.H. Caldwell, K.L. Schaller, R.S. Lasher, E. Peles, and S.R. Levinson Sodium channel Na(v)1.6 is localized at nodes of Ranvier, dendrites, and synapses Proc Natl Acad Sci U S A 97 2000 5616 5620
8. G occupy a different postsynaptic domain from acetylcholine receptors from an early stage of neuromuscular junction maturation in rats J Neurosci 23 2003 2102 2111
9. S.A. Cohen Immunocytochemical localization of rH1 sodium channel in adult rat heart atria and ventricle. Presence in terminal intercalated disks Circulation 94 1996 3083 3086
10. J.D. Malhotra, C. Chen, I. Rivolta, H. Abriel, R. Malhotra, and L.N. Mattei Characterization of sodium channel α and β subunits in rat and mouse cardiac myocytes Circulation 103 2001 1303 1310
11. S.K. Maier, R.E. Westenbroek, K.A. Schenkman, E.O. Feigl, T. Scheuer, and W.A. Catterall An unexpected role for brain-type sodium channels in coupling of cell surface depolarization to contraction in the heart Proc Natl Acad Sci U S A 99 2002 4073 4078
12. S.K. Maier, R.E. Westenbroek, T.T. Yamanushi, H. Dobrzynski, M.R. Boyett, and W.A. Catterall An unexpected requirement for brain-type sodium channels for control of heart rate in the mouse sinoatrial node Proc Natl Acad Sci U S A 100 2003 3507 3512
13. A.L. Goldin, R.L. Barchi, J.H. Caldwell, F. Hofmann, J.R. Howe, and J.C. Hunter Nomenclature of voltage-gated sodium channels Neuron 28 2000 365 368
14. P.C. Viswanathan, and J.R. Balser Inherited sodium channelopathies: a continuum of channel dysfunction Trends Cardiovasc Med 14 2004 28 35
15. R. Robinson, and M. Gardiner Molecular basis of Mendelian idiopathic epilepsies Ann Med 36 2004 89 97
16. J. Lai, F. Porreca, J.C. Hunter, and M.S. Gold Voltage-gated sodium channels and hyperalgesia Annu Rev Pharmacol Toxicol 44 2004 371 397
17. F.H. Yu, and W.A. Catterall Overview of the voltage-gated sodium channel family Genome Biol 4 2003 207
18. H.L. Tan, C.R. Bezzina, J.P. Smits, A.O. Verkerk, and A.A. Wilde Genetic control of sodium channel function Cardiovasc Res 57 2003 961 973
19. H. Liu, C. Clancy, J. Cormier, and R. Kass Mutations in cardiac sodium channels: clinical implications Am J Pharmacogenomics 3 2003 173 179
20. N.W. Plummer, and M.H. Meisler Evolution and diversity of mammalian sodium channel genes Genomics 57 1999 323 331
21. S.K. Maier, R.E. Westenbroek, K.A. McCormick, R. Curtis, T. Scheuer, and W.A. Catterall Distinct subcellular localization of different sodium channel alpha and beta subunits in single ventricular myocytes from mouse heart Circulation 109 2004 1421 1427
22. H.A. Hartmann, L.V. Colom, M.L. Sutherland, and J.L. Noebels Selective localization of cardiac SCN5A sodium channels in limbic regions of rat brain Nature 2 1999 593 595
23. L. Wu, K. Nishiyama, J.G. Hollyfield, and Q. Wang Localization of Nav1.5 sodium channel protein in the mouse brain Neuroreport 13 2002 2547 2551
24. J. Britton Syncope and seizures. Differential diagnosis and evaluation Clin Auton Res 14 2004 148 159
25. L.L. Isom, K.S. De Jhong, D.E. Patton, B.F.X. Reber, J. Offord, and H. Charbonneau Primary structure and functional expression of the β1 subunit of the rat brain sodium channel Science 256 1992 839 842
26. L.L. Isom, D.S. Ragsdale, K.S. De Jhong, R.E. Westenbroek, B.F. Reber, and T. Scheuer Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif Cell 83 1995 433 442
27. K. Morgan, E.B. Stevens, B. Shah, P.J. Cox, A.K. Dixon, and K. Lee 3β: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics Proc Natl Acad Sci U S A 97 2000 2308 2313
28. K.A. Kazen-Gillespie, D.S. Ragsdale, M.R. D'Andrea, L.N. Mattei, K.E. Rogers, and L.L. Isom Cloning, localization, and functional expression of sodium channel β1A subunits J Biol Chem 275 2000 1079 1088
29. + channel subunits and Ig domains Nature 383 1996 307 308
30. F.H. Yu, R.E. Westenbroek, I. Silos-Santiago, K.A. McCormick, D. Lawson, and P. Ge Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2 J Neurosci 23 2003 7577 7585
31. + channel function in the extracellular domain of the β1 subunit J Biol Chem 273 1998 3954 3962
32. L.L. Isom, K.S. De Jongh, and W.A. Catterall Auxiliary subunits of voltage-gated ion channels Neuron 12 1994 1183 1194
33. L.L. Isom, T. Scheuer, A.B. Brownstein, D.S. Ragsdale, B.J. Murphy, and W.A. Catterall Functional co-expression of the β1 and type IIA α subunits of sodium channels in a mammalian cell line J Biol Chem 270 1995 3306 3312
34. L. Sangameswaran, S.G. Delgado, L.M. Fish, B.D. Koch, L.B. Jakeman, and G.R. Stewart Structure and function of a novel voltage-gated, tetrodotoxin-resistant sodium channel specific to sensory neurons J Biol Chem 271 1996 5953 5956
35. K. Vijayaragavan, M.E. O'Leary, and M. Chahine Gating properties of Na(v)1.7 and Na(v)1.8 peripheral nerve sodium channels J Neurosci 21 2001 7909 7918
36. K. Vijayaragavan, A.J. Powell, I.J. Kinghorn, and M. Chahine Role of auxiliary beta1-, beta2-, and beta3-subunits and their interaction with Na(v)1.8 voltage-gated sodium channel Biochem Biophys Res Commun 319 2004 531 540
37. Y. Qu, L.L. Isom, R.E. Westenbroek, J.C. Rogers, T.N. Tanada, and K.A. McCormick Modulation of cardiac Na+ channel expression in Xenopus oocytes by β1 subunits J Biol Chem 270 1995 25696 25701
38. + channel β1 subunit mRNA expressed in adult human skeletal muscle, heart, and brain is encoded by a single gene J Biol Chem 269 1994 7571 7578
39. J.S. Yang, P.B. Bennett, N. Makita, A.L. George, and R.L. Barchi Expression of the sodium channel β1 subunit in rat skeletal muscle is selectively associated with the tetrodotoxin-sensitive α subunit isoform Neuron 11 1993 915 922
40. H.B. Nuss, N. Chiamvimonvat, M.T. Perez-Garcia, G.F. Tomaselli, and E. Marban Functional association of the beta 1 subunit with human cardiac (hH1) and rat skeletal muscle (μ1) sodium channel alpha subunits expressed in Xenopus oocytes J Gen Physiol 106 1995 1171 1191
41. J.C. Makielski, J.T. Limberis, S.Y. Chang, Z. Fan, and J.W. Kyle Coexpression of beta 1 with cardiac sodium channel alpha subunits in oocytes decreases lidocaine block Mol Pharmacol 49 1996 30 39
42. + channel activity through interactions between alpha- and beta1-subunits Circ Res 83 1998 141 146
43. S.H. Ko, P.W. Lenkowski, H.C. Lee, J.P. Mounsey, and M.K. Patel Modulation of Na(v)1.5 by beta1- and beta3-subunit co-expression in mammalian cells Pflugers Arch 449 2005 403 412
44. A.I. Fahmi, M. Patel, E.B. Stevens, A.L. Fowden, J.E. John III, and K Lee The sodium channel beta-subunit SCN3b modulates the kinetics of SCN5a and is expressed heterogeneously in sheep heart J Physiol 537 2001 693 700
45. J.D. Malhotra, V. Thyagarajan, C. Chen, and L.L. Isom Tyrosine-phosphorylated- and nonphosphorylated-sodium channel β1 subunits are differentially localized in cardiac myocytes J Biol Chem 279 2004 40748 40754
46. J.N. Dominguez, F. Navarro, D. Franco, R.P. Thompson, and A.E. Aranega Temporal and spatial expression pattern of beta1 sodium channel subunit during heart development Cardiovasc Res 65 2005 842 850
47. T. Zimmer, C. Biskup, C. Bollensdorff, and K. Benndorf 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 2002 13 21
48. J.S. Rougier, M.X. van Bemmelen, M.C. Bruce, T. Jespersen, B. Gavillet, and F. Apotheloz Molecular determinants of voltage-gated sodium channel regulation by the Nedd4/Nedd4-like proteins Am J Physiol Cell Physiol 288 2005 C692 C701
49. M.X. van Bemmelen, J.S. Rougier, B. Gavillet, F. Apotheloz, D. Daidie, and M. Tateyama Cardiac voltage-gated sodium channel Nav1.5 is regulated by Nedd4-2 mediated ubiquitination Circ Res 95 2004 284 291
50. V. Blot, F. Perugi, B. Gay, M.C. Prevost, L. Briant, and F. Tangy Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding J Cell Sci 117 2004 2357 2367
51. T.M. Grieco, J.D. Malhotra, C. Chen, L.L. Isom, and I.M. Raman Open-channel block by the cytoplasmic tail of sodium channel β4 as a mechanism for resurgent sodium current Neuron 45 2005 233 244
52. v1.1 channel: a mouse model for severe myoclonic epilepsy of infancy Abstract viewer/itinerary planner 2004 Society for Neuroscience Washington, DC 5 Program No. 479
53. L. Claes, J. Del-Favero, B. Ceulemans, L. Lagae, C. Van Broeckhoven, and P. De Jonghe De novo mutations in the sodium-channel gene SCN1A cause severe myoclonic epilepsy of infancy Am J Hum Genet 68 2001 1327 1332
54. G.A. Papadatos, P.M. Wallerstein, C.E. Head, R. Ratcliff, P.A. Brady, and K. Benndorf Slowed conduction and ventricular tachycardia after targeted disruption of the cardiac sodium channel gene Scn5a Proc Natl Acad Sci U S A 99 2002 6210 6215
55. A. Escayg, A. Heils, B.T. MacDonald, K. Haug, T. Sander, and M.H. Meisler A novel scn1a mutation associated with generalized epilepsy with febrile seizures plus- and prevalence of various patients with epilepsy Am J Hum Genet 68 2001 866 873
56. J.A. Kearney, D.A. Buchner, G. De Haan, M. Adamska, S.I. Levin, and A.R. Furay Molecular and pathological effects of a modifier gene on deficiency of the sodium channel Scn8a (Na(v)1.6) Hum Mol Genet 11 2002 2765 2775
57. L.K. Sprunger, A. Escayg, S. Tallaksen-Greene, R.L. Albin, and M.H. Meisler Dystonia associated with mutation of the neuronal sodium channel Scn8a and identification of the modifier locus Scnm1 on mouse chromosome 3 Hum Mol Genet 8 1999 471 479
58. M. Hamann, M.H. Meisler, and A. Richter Motor disturbances in mice with deficiency of the sodium channel gene Scn8a show features of human dystonia Exp Neurol 184 2003 830 838
59. T.L. Yarbrough, T. Lu, H.C. Lee, and E.F. Shibata Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude Circ Res 90 2002 443 449
60. C. Chen, B. Bharucha, Y. Chen, R.E. Westenbroek, A. Brown, and J.D. Malhotra Reduced sodium channel density, altered voltage dependence of inactivation, and increased susceptibility to seizures in mice lacking sodium channel β2 subunits Proc Natl Acad Sci U S A 99 2002 17072 17077
61. C. Chen, R.E. Westenbroek, X. Xu, C.A. Edwards, D.R. Sorenson, and Y. Chen Mice lacking sodium channel β1 subunits display defects in neuronal excitability, sodium channel expression, and nodal architecture J Neurosci 24 2004 4030 4042
62. L.L. Isom The role of sodium channels in cell adhesion Front Biosci 7 2002 12 23
63. J. Srinivasan, M. Schachner, and W.A. Catterall Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R Proc Natl Acad Sci U S A 95 1998 15753 15757
64. Z.-C. Xiao, D.S. Ragsdale, J.D. Malhorta, L.N. Mattei, P.E. Braun, and M. Schachner Tenascin-R is a functional modulator of sodium channel β subunits J Biol Chem 274 1999 26511 26517
65. M.W. Schellings, Y.M. Pinto, and S. Heymans Matricellular proteins in the heart: possible role during stress and remodeling Cardiovasc Res 64 2004 24 31
66. T. Brümmendorf, M. Hubert, U. Treubert, R. Leuschner, A. Tarnok, and F.G. Rathjen The axonal recognition molecule F11 is a multifunctional protein: specific domains mediate interactions with Ng-CAM and restrictin Neuron 10 1993 711 727
67. J.D. Malhotra, K. Kazen-Gillespie, M. Hortsch, and L.L. Isom Sodium channel β subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact J Biol Chem 275 2000 11383 11388
68. P.J. Mohler, J.J. Schott, A.O. Gramolini, K.W. Dilly, S. Guatimosim, and W.H. duBell Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death Nature 421 2003 634 639
69. P.J. Mohler, I. Rivolta, C. Napolitano, G. LeMaillet, S. Lambert, and S.G. Priori Nav1.5 E1053K mutation causing Brugada syndrome blocks binding to ankyrin-G and expression of Nav1.5 on the surface of cardiomyocytes Proc Natl Acad Sci U S A 101 2004 17533 17538
70. V.S. Chauhan, S. Tuvia, M. Buhusi, V. Bennett, and A.O. Grant Abnormal cardiac Na(+) channel properties and QT heart rate adaptation in neonatal ankyrin(B) knockout mice Circ Res 86 2000 441 447
71. D. Zhou, S. Lambert, P.J. Malen, S. Carpenter, L.M. Boland, and V. Bennett AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing J Cell Biol 143 1998 1295 1304
72. P. Scotland, D. Zhou, H. Benveniste, and V. Bennett Nervous system defects of AnkyrinB (-/-) mice suggest functional overlap between the cell adhesion molecule L1 and 440-kD AnkyrinB in premyelinated axons J Cell Biol 143 1998 1305 1315
73. J.D. Malhotra, M.C. Koopmann, K.A. Kazen-Gillespie, N. Fettman, M. Hortsch, and L.L. Isom Structural requirements for interaction of sodium channel β1 subunits with ankyrin J Biol Chem 277 2002 26681 26688
74. D.P. McEwen, L.S. Meadows, C. Chen, V. Thyagarajan, and L.L. Isom Sodium channel β1 subunit-mediated modulation of Nav1.2 currents and cell surface density is dependent on interactions with contactin and ankyrin J Biol Chem 279 2004 16044 16049
75. D.P. McEwen, and L.L. Isom Heterophilic interactions of sodium channel beta 1 subunits with axonal and glial cell adhesion molecules J Biol Chem 279 2004 52744 52752
76. K. Kazarinova-Noyes, J.D. Malhotra, D.P. McEwen, L.N. Mattei, E.O. Berglund, and B. Ranscht Contactin associates with Na+ channels and increases their functional expression J Neurosci 21 2001 7517 7525
77. K. Kazarinova-Noyes, and P. Shrager Molecular constituents of the node of Ranvier Mol Neurobiol 26 2002 167 182
78. C.F. Ratcliffe, R.E. Westenbroek, R. Curtis, and W.A. Catterall Sodium channel beta1 and beta3 subunits associate with neurofascin through their extracellular immunoglobulin-like domain J Cell Biol 154 2001 427 434
79. B.S. Shah, A.M. Rush, S. Liu, L. Tyrrell, J.A. Black, and S.D. Dib-Hajj Contactin associates with sodium channel Nav1.3 in native tissues and increases channel density at the cell surface J Neurosci 24 2004 7387 7399
80. C.J. Liu, S.D. Dib-Hajj, J.A. Black, J. Greenwood, Z. Lian, and S.G. Waxman Direct interaction with contactin targets voltage-gated sodium channel Na(v)1.9/NaN to the cell membrane J Biol Chem 276 2001 46553 46561
81. A.P. Soler, G. Gilliard, Y. Xiong, K.A. Knudsen, J.L. Martin, and C.B. De Suarez Overexpression of neural cell adhesion molecule in Chagas' myocarditis Hum Pathol 32 2001 149 155
82. S. Gattenlohner, C. Waller, G. Ertl, B.D. Bultmann, H.K. Muller-Hermelink, and A. Marx NCAM(CD56) and RUNX1(AML1) are up-regulated in human ischemic cardiomyopathy and a rat model of chronic cardiac ischemia Am J Pathol 163 2003 1081 1090
83. C.F. Ratcliffe, Y. Qu, K.A. McCormick, V.C. Tibbs, J.E. Dixon, and T. Scheuer A sodium channel signaling complex: modulation by associated receptor protein tyrosine phosphatase beta Nat Neurosci 3 2000 437 444
84. L.S. Meadows, J. Malhotra, A. Loukas, V. Thyagarajan, K.A. Kazen-Gillespie, and M.C. Koopman Functional and biochemical analysis of a sodium channel β1 subunit mutation responsible for generalized epilepsy with febrile seizures plus type 1 J Neurosci 22 2002 10699 10709
85. S.M. Jenkins, K. Kizhatil, N.R. Kramarcy, A. Sen, R. Sealock, and V. Bennett FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons J Cell Sci 114 2001 3823 3835
86. X. Zhang, J.Q. Davis, S. Carpenter, and V. Bennett Structural requirements for association of neurofascin with ankyrin J Biol Chem 273 1998 30785 30794
87. T.D. Garver, Q. Ren, S. Tuvia, and V. Bennett Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin J Cell Biol 137 1997 703 714
88. S. Tuvia, T.D. Garver, and V. Bennett The phosphorylation state of the FIGQY tyrosine of neurofascin determines ankyrin-binding activity and patterns of cell segregation Proc Natl Acad Sci U S A 94 1997 12957 12962
89. L. Chen, B. Ong, and V. Bennett LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling J Cell Biol 154 2001 841 855
90. F. Brette, and C. Orchard T-tubule function in mammalian cardiac myocytes Circ Res 92 2003 1182 1192
91. H.W. Sinn, J. Balsamo, J. Lilien, and J.J. Lin Localization of the novel Xin protein to the adherens junction complex in cardiac and skeletal muscle during development Dev Dyn 225 2002 1 13
92. N.S. Peters, N.J. Severs, S.M. Rothery, C. Lincoln, M.H. Yacoub, and C.R. Green Spatiotemporal relation between gap junctions and fascia adherens junctions during postnatal development of human ventricular myocardium Circulation 90 1994 713 725
93. S. Kostin, S. Hein, E.P. Bauer, and J. Schaper Spatiotemporal development and distribution of intercellular junctions in adult rat cardiomyocytes in culture Circ Res 85 1999 154 167
94. J. Lilien, J. Balsamo, C. Arregui, and G. Xu Turn-off, drop-out: functional state switching of cadherins Dev Dyn 224 2002 18 29
95. V.A. Maltsev, and A.I. Undrovinas Cytoskeleton modulates coupling between availability and activation of cardiac sodium channel Am J Physiol 273 1997 H1832 H1840
96. A.I. Undrovinas, G.S. Shander, and J.C. Makielski Cytoskeleton modulates gating of voltage-dependent sodium channel in heart Am J Physiol 269 1995 H203 H214
97. Y. Ou, P. Strege, S.M. Miller, J. Makielski, M. Ackerman, and S.J. Gibbons Syntrophin gamma 2 regulates SCN5A gating by a PDZ domain-mediated interaction J Biol Chem 278 2003 1915 1923
98. R.J. Barker, R.L. Price, and R.G. Gourdie Increased co-localization of connexin43 and ZO-1 in dissociated adult myocytes Cell Commun Adhes 8 2001 205 208
99. R.J. Barker, R.L. Price, and R.G. Gourdie Increased association of ZO-1 with connexin43 during remodeling of cardiac gap junctions Circ Res 90 2002 317 324
100. T. Zimmer, and K. Benndorf The human heart and rat brain IIA Na(+) channels interact with different molecular regions of the beta(1) subunit J Gen Physiol 120 2002 887 895
101. J. Spampanato, J.A. Kearney, G. De Haan, D.P. McEwen, A. Escayg, and I. Aradi A novel epilepsy mutation in the sodium channel SCN1A identifies a cytoplasmic domain for beta subunit interaction J Neurosci 24 2004 10022 10034
102. T.J. Jentsch, C.A. Hubner, and J.C. Fuhrmann Ion channels: function unravelled by dysfunction Nat Cell Biol 6 2004 1039 1047
103. Y. Yang, Y. Wang, S. Li, Z. Xu, H. Li, and L. Ma Mutations in SCN9A, encoding a sodium channel alpha subunit, in patients with primary erythermalgia J Med Genet 41 2004 171 174
104. +-channel beta1 subunit gene SCN1B Nat Genet 19 1998 366 370
105. D. Audenaert, L. Claes, B. Ceulemans, A. Lofgren, C. Van Broeckhoven, and P. De Jonghe A deletion in SCN1B is associated with febrile seizures and early-onset absence epilepsy Neurology 61 2003 854 856
106. X. Wan, Q. Wang, and G.E. Kirsch Functional suppression of sodium channels by beta(1)-subunits as a molecular mechanism of idiopathic ventricular fibrillation J Mol Cell Cardiol 32 2000 1873 1884
107. G.W. Abbott, and S.A.N. Goldstein A superfamily of small potassium channel subunits: form and function of the MinK-related peptides (MiRPs) Q Rev Biophys 31 1998 357 398
108. J. Wei, D.W. Wang, M. Alings, F. Fish, M. Wathen, and D.M. Roden Congenital long-QT syndrome caused by a novel mutation in a conserved acidic domain of the cardiac Na+ channel [in process citation] Circulation 99 1999 3165 3171
109. Y. Qu, J.C. Rogers, S.F. Chen, K.A. McCormick, T. Scheuer, and W.A. Catterall Functional roles of the extracellular segments of the sodium channel alpha subunit in voltage-dependent gating and modulation by beta1 subunits J Biol Chem 274 1999 32647 32654
110. K.A. McCormick, J. Srinivasan, K. White, T. Scheuer, and W.A. Catterall The extracellular domain of the beta1 subunit is both necessary and sufficient for beta1-like modulation of sodium channel gating J Biol Chem 274 1999 32638 32646
111. L.S. Meadows, C. Chen, A.I. Speelman, J.D. Malhotra, and L.L. Isom Characterization of cardiac sodium channel function in β1 subunit null mice Abstract viewer/itinerary planner 2004 Society for Neuroscience Washington, DC Program No. 262.9. 2004
112. S. Kaab, J. Dixon, J. Duc, D. Ashen, M. Nabauer, and D.J. Beuckelmann Molecular basis of transient outward potassium current downregulation in human heart failure: a decrease in Kv4.3 mRNA correlates with a reduction in current density Circulation 98 1998 1383 1393
113. I. Deschenes, and G.F. Tomaselli Modulation of Kv4.3 current by accessory subunits FEBS Lett 528 2002 183 188
114. I. Deschenes, A.A. Armoundas, S.P. Jones, S. Poelzing, and G.F. Tomaselli Functional link between Na channels and Ito revealed by posttranscriptional gene silencing of Nav-beta1 in cardiac myocytes AHA Sci Sess (Abstr) 283 2004
115. I. Deschenes, A.A. Armoundas, S.P. Jones, and G.F. Tomaselli Post-transcriptional gene silencing of KChIP2 in cardiac myocytes suggests a structural and developmental link between Ito and Na channel AHA Sci Sess (Abstr) 234 2003
116. G. Lemaillet, B. Walker, and S. Lambert Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits J Biol Chem 278 2003 27333 27339
117. P.J. Mohler, I. Splawski, C. Napolitano, G. Bottelli, L. Sharpe, and K. Timothy A cardiac arrhythmia syndrome caused by loss of ankyrin-B function Proc Natl Acad Sci U S A 101 2004 9137 9142
118. J.M. Ervasti, K. Ohlendieck, S.D. Kahl, M.G. Gaver, and K.P. Campbell Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle Nature 345 1990 315 319
119. S.H. Gee, R. Madhavan, S.R. Levinson, J.H. Caldwell, R. Sealock, and S.C. Froehner Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins J Neurosci 18 1998 128 137
120. D. Leonoudakis, L.R. Conti, S. Anderson, C.M. Radeke, L.M. McGuire, and M.E. Adams Protein trafficking and anchoring complexes revealed by proteomic analysis of inward rectifier potassium channel (Kir2.x)-associated proteins J Biol Chem 279 2004 22331 22346
121. + channel subtypes in central neurons Neuron 3 1989 695 704
122. T. Furuyama, Y. Morita, S. Inagaki, and H. Takagi Distribution of I, II and III subtypes of voltage-sensitive Na+ channel mRNA in the rat brain Brain Res Mol Brain Res 17 1993 169 173
123. K.L. Schaller, D.M. Krzemien, P.J. Yarowsky, B.K. Krueger, and J.H. Caldwell A novel, abundant sodium channel expressed in neurons and glia J Neurosci 15 1995 3231 3242
124. D.M. Barry, J.S. Trimmer, J.P. Merlie, and J.M. Nerbonne Differential expression of voltage-gated K+ channel subunits in adult rat heart. Relation to functional K+ channels? Circ Res 77 1995 361 369
125. S. Takeuchi, Y. Takagishi, K. Yasui, Y. Murata, J. Toyama, and I. Kodama Voltage-gated K(+)Channel, Kv4.2, localizes predominantly to the transverse-axial tubular system of the rat myocyte J Mol Cell Cardiol 32 2000 1361 1369