Channelopathies from mutations in the cardiac sodium channel protein complex

Journal of Molecular and Cellular Cardiology

Volumn 61, Issue , 2013, Pages 34-43

  Adsit, Graham S ^a   Vaidyanathan, Ravi ^a   Galler, Carla M ^b   Kyle, John W ^a   Makielski, Jonathan C ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b Madison College   (United States)

Author keywords

Arrhythmia; Brugada Syndrome; Long QT syndrome; SCN5A; SIDS; Sodium current

Indexed keywords

ALPHA ACTININ 2; ANKYRIN; ANKYRIN G; CALMODULIN; CARRIER PROTEIN; CAVEOLIN 3; CONNEXIN 40; CONNEXIN 43; DESMOGLEIN 2; DYSTROPHIN; FIBROBLAST GROWTH FACTOR; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; MEMBRANE PROTEIN; MULTICOPY SUPPRESSOR OF GSP1; PLAKOPHILIN; PLAKOPHILIN 2; PROTEIN 14 3 3; PROTEIN 14 3 3 ETA; SODIUM; SODIUM CHANNEL; SODIUM CHANNEL NAV1.5; SYNAPSE ASSOCIATED PROTEIN 97; SYNTROPHIN; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; UTROPHIN; VOLTAGE GATED SODIUM CHANNEL BETA 1 SUBUNIT; VOLTAGE GATED SODIUM CHANNEL BETA 2 SUBUNIT; VOLTAGE GATED SODIUM CHANNEL BETA 3 SUBUNIT; VOLTAGE GATED SODIUM CHANNEL BETA 4 SUBUNIT;

BRUGADA SYNDROME; CHANNEL GATING; DISEASE ASSOCIATION; GENE; GENE MUTATION; HEART ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART MUSCLE CONDUCTION DISTURBANCE; HEART MUSCLE EXCITABILITY; HEART VENTRICLE FIBRILLATION; HUMAN; INHERITANCE; LONG QT SYNDROME; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SCN5A GENE; SICK SINUS SYNDROME; SODIUM CHANNELOPATHY; SODIUM CURRENT; SUDDEN INFANT DEATH SYNDROME;

ARRHYTHMIA; BRUGADA SYNDROME; LONG QT SYNDROME; SCN5A; SIDS; SODIUM CURRENT;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM-BINDING PROTEINS; CHANNELOPATHIES; HOMEOSTASIS; HUMANS; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES; MUSCLE PROTEINS; MUTATION, MISSENSE; MYOCARDIAL CONTRACTION; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PROTEIN SUBUNITS;

EID: 84880333897     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.03.017     Document Type: Review

References (135)

1. Qu Y., Rogers J.C., Chen S.F., McCormick K.A., Scheuer T., Catterall W.A. Functional roles of the extracellular segments of the sodium channel α subunit in voltage-dependent gating and modulation by β1 subunits. J Biol Chem Nov 12 1999, 274(46):32647-32654.
2. Allouis M., Le Bouffant F., Wilders R., Peroz D., Schott J.J., Noireaud J., et al. 14-3-3 is a regulator of the cardiac voltage-gated sodium channel Nav1.5. Circ Res Jun 23 2006, 98(12):1538-1546.
3. Dhar M.J., Chen C., Rivolta I., Abriel H., Malhotra R., Mattei L.N., et al. Characterization of sodium channel alpha- and beta-subunits in rat and mouse cardiac myocytes. Circulation Mar 6 2001, 103(9):1303-1310.
4. +) current in human ventricle: implications for sodium loading and homeostasis. J Cardiovasc Electrophysiol May 2006, 17(Suppl. 1):S15-S20.
5. Valdivia C.R., Nagatomo T., Makielski J.C. Late currents affect kinetics for heart and skeletal Na channel α and β1 subunits expressed in HEK293 cells. J Mol Cell Cardiol Aug 2002, 34(8):1029-1039.
6. Antzelevitch C. The Brugada syndrome: ionic basis and arrhythmia mechanisms. J Cardiovasc Electrophysiol Feb 2001, 12(2):268-272.
7. + channel mutation leading to loss of function and non-progressive cardiac conduction defects. J Mol Cell Cardiol May 2003, 35(5):549-557.
8. + current from a canine heart failure model and from human heart failure. Biophys J 2000, 78:523. [Ref Type: Abstract].
9. + channel isoform Nav1.5 is modulated by its beta1 subunit. J Physiol Sci May 2009, 59(3):217-225.
10. Nuss H.B., Chiamvimonvat N., Perez-Garcia M.T., Tomaselli G.F., Marban E. Functional association of the β1 subunit with human cardiac (hH1) and rat skeletal muscle (μ1) sodium channel α subunits expressed in Xenopus oocytes. J Gen Physiol Dec 1995, 106(6):1171-1191.
11. Ziane R., Huang H., Moghadaszadeh B., Beggs A.H., Levesque G., Chahine M. Cell membrane expression of cardiac sodium channel Na(v)1.5 is modulated by alpha-actinin-2 interaction. Biochemistry Jan 12 2010, 49(1):166-178.
12. Goldin A.L., Barchi R.L., Caldwell J.H., Hofmann F., Howe J.R., Hunter J.C., et al. Nomenclature of voltage-gated sodium channels. Neuron Nov 2000, 28(2):365-368.
13. Watanabe H., Koopmann T.T., Le Scouarnec S., Yang T., Ingram C.R., Schott J.J., et al. Sodium channel beta1 subunit mutations associated with Brugada syndrome and cardiac conduction disease in humans. J Clin Invest Jun 2008, 118(6):2260-2268.
14. Maier S.K., Westenbroek R.E., Schenkman K.A., Feigl E.O., Scheuer T., Catterall W.A. 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 Mar 19 2002, 99(6):4073-4078.
15. Lowe J.S., Palygin O., Bhasin N., Hund T.J., Boyden P.A., Shibata E., et al. Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J Cell Biol Jan 14 2008, 180(1):173-186.
16. Balser J.R. The cardiac sodium channel: gating function and molecular pharmacology. J Mol Cell Cardiol Apr 2001, 33(4):599-613.
17. Catterall W.A. From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron Apr 2000, 26(1):13-25.
18. Lopez-Santiago L.F., Meadows L.S., Ernst S.J., Chen C., Malhotra J.D., Mcewen D.P., et al. Sodium channel Scn1b null mice exhibit prolonged QT and RR intervals. J Mol Cell Cardiol Aug 10 2007, 43(5):636-647.
19. Mohler P.J., Rivolta I., Napolitano C., LeMaillet G., Lambert S., Priori S.G., et al. 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 Dec 14 2004, 101(50):17533-17538.
20. Bennett P.B., Yazawa K., Makita N., GeorgeJr A.L. Molecular mechanism for an inherited cardiac arrhythmia. Nature 1995, 376:683-685.
21. +/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovasc Res Feb 1 2010, 85(3):454-463.
22. Watanabe H., Darbar D., Kaiser D.W., Jiramongkolchai K., Chopra S., Donahue B.S., et al. Mutations in sodium channel beta1- and beta2-subunits associated with atrial fibrillation. Circ Arrhythm Electrophysiol Jun 2009, 2(3):268-275.
23. Ruan Y., Liu N., Priori S.G. Sodium channel mutations and arrhythmias. Nat Rev Cardiol May 2009, 6(5):337-348.
24. Wilde A.A., Brugada R. Phenotypical manifestations of mutations in the genes encoding subunits of the cardiac sodium channel. Circ Res Apr 1 2011, 108(7):884-897.
25. Hund T.J., Koval O.M., Li J., Wright P.J., Qian L., Snyder J.S., et al. A beta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest Oct 2010, 120(10):3508-3519.
26. Ackerman M.J., Siu B.L., Sturner W.Q., Tester D.J., Valdivia C.R., Makielski J.C., et al. Postmortem molecular analysis of SCN5A defects in sudden infant death syndrome. JAMA Nov 14 2001, 286(18):2264-2269.
27. Komada M., Soriano P. [Beta]IV-spectrin regulates sodium channel clustering through ankyrin-G at axon initial segments and nodes of Ranvier. J Cell Biol Jan 21 2002, 156(2):337-348.
28. Hu D., Barajas-Martinez H., Medeiros-Domingo A., Crotti L., Veltmann C., Schimpf R., et al. A novel rare variant in SCN1Bb linked to Brugada syndrome and SIDS by combined modulation of Na(v)1.5 and K(v)4.3 channel currents. Heart Rhythm May 2012, 9(5):760-769.
29. Olson T.M., Michels V.V., Ballew J.D., Reyna S.P., Karst M.L., Herron K.J., et al. Sodium channel mutations and susceptibility to heart failure and atrial fibrillation. JAMA Jan 26 2005, 293(4):447-454.
30. Cheng J., Morales A., Siegfried J.D., Li D., Norton N., Song J., et al. 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 Dec 2010, 3(6):287-294.
31. Mazzone A., Strege P.R., Tester D.J., Bernard C.E., Faulkner G., De Giorgio R., et al. A mutation in telethonin alters Nav1.5 function. J Biol Chem Jun 13 2008, 283(24):16537-16544.
32. Chagot B., Chazin W.J. Solution NMR structure of Apo-calmodulin in complex with the IQ motif of human cardiac sodium channel NaV1.5. J Mol Biol Feb 11 2011, 406(1):106-119.
33. Potet F., Chagot B., Anghelescu M., Viswanathan P.C., Stepanovic S.Z., Kupershmidt S., et al. Functional interactions between distinct sodium channel cytoplasmic domains through the action of calmodulin. J Biol Chem Mar 27 2009, 284(13):8846-8854.
34. + channel alpha and beta2 subunits. J Biol Chem Nov 9 2012, 287(46):39061-39069.
35. Meadows L.S., Isom L.L. Sodium channels as macromolecular complexes: implications for inherited arrhythmia syndromes. Cardiovasc Res Aug 15 2005, 67(3):448-458.
36. Catterall W.A. Signaling complexes of voltage-gated sodium and calcium channels. Neurosci Lett Dec 10 2010, 486(2):107-116.
37. Gaborit N., Steenman M., Lamirault G., Le Meur N., Le Bouter S., Lande G., et al. Human atrial ion channel and transporter subunit gene-expression remodeling associated with valvular heart disease and atrial fibrillation. Circulation Jul 26 2005, 112(4):471-481.
38. Johnson D., Bennett E.S. Isoform-specific effects of the beta2 subunit on voltage-gated sodium channel gating. J Biol Chem Sep 8 2006, 281(36):25875-25881.
39. + sensitivity of sodium channels. J Biol Chem Oct 22 2004, 279(43):45004-45012.
40. Mishra S., Undrovinas N.A., Maltsev V.A., Reznikov V., Sabbah H.N., Undrovinas A. Post-transcriptional silencing of SCN1B and SCN2B genes modulates late sodium current in cardiac myocytes from normal dogs and dogs with chronic heart failure. Am J Physiol Heart Circ Physiol Oct 2011, 301(4):H1596-H1605.
41. Abriel H. Cardiac sodium channel Na(v)1.5 and interacting proteins: physiology and pathophysiology. J Mol Cell Cardiol Sep 8 2009, 48(1):2-11.
42. Shy D., Gillet L., Abriel H. Cardiac sodium channel Na(V)1.5 distribution in myocytes via interacting proteins: the multiple pool model. Biochim Biophys Acta Oct 31 2012, 1833(4):886-894.
43. Olesen M.S., Holst A.G., Svendsen J.H., Haunso S., Tfelt-Hansen J. SCN1Bb R214Q found in 3 patients: 1 with Brugada syndrome and 2 with lone atrial fibrillation. Heart Rhythm May 2012, 9(5):770-773.
44. Tan H.L., Kupershmidt S., Zhang R., Stepanovic S., Roden D.M., Wilde A.A., et al. A calcium sensor in the sodium channel modulates cardiac excitability. Nature Jan 24 2002, 415(6870):442-447.
45. Petitprez S., Zmoos A.F., Ogrodnik J., Balse E., Raad N., El Haou S., et al. SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ Res Feb 4 2011, 108(3):294-304.
46. + channel in cardiac disease. Circulation Oct 23 2012, 126(17):2084-2094.
47. Lin X., Liu N., Lu J., Zhang J., Anumonwo J.M., Isom L.L., et al. Subcellular heterogeneity of sodium current properties in adult cardiac ventricular myocytes. Heart Rhythm 2011 Dec, 8(12):1923-1930.
48. Goldin A.L. Mechanisms of sodium channel inactivation. Curr Opin Neurobiol Jun 2003, 13(3):284-290.
49. Jansen J.A., Noorman M., Musa H., Stein M., de Jong S., van der N.R., et al. Reduced heterogeneous expression of Cx43 results in decreased Nav1.5 expression and reduced sodium current that accounts for arrhythmia vulnerability in conditional Cx43 knockout mice. Heart Rhythm Apr 2012, 9(4):600-607.
50. Hakim P., Brice N., Thresher R., Lawrence J., Zhang Y., Jackson A.P., et al. Scn3b knockout mice exhibit abnormal sino-atrial and cardiac conduction properties. Acta Physiol (Oxf) Jan 2010, 198(1):47-59.
51. Fahmi A.I., Patel M., Stevens E.B., Fowden A.L., John J.E., Lee K., et al. The sodium channel beta-subunit SCN3b modulates the kinetics of SCN5a and is expressed heterogeneously in sheep heart. J Physiol Dec 15 2001, 537(Pt 3):693-700.
52. Milstein M.L., Musa H., Balbuena D.P., Anumonwo J.M., Auerbach D.S., Furspan P.B., et al. Dynamic reciprocity of sodium and potassium channel expression in a macromolecular complex controls cardiac excitability and arrhythmia. Proc Natl Acad Sci U S A Jul 31 2012, 109(31):E2134-E2143.
53. van der Velden H.M., Jongsma H.J. Cardiac gap junctions and connexins: their role in atrial fibrillation and potential as therapeutic targets. Cardiovasc Res May 2002, 54(2):270-279.
54. Undrovinas A.I., Fleidervish I.A., Makielski J.C. Inward sodium current at resting potentials in single cardiac myocytes induced by the ischemic metabolite lysophosphatidylcholine. Circ Res Nov 1992, 71(5):1231-1241.
55. Olesen M.S., Jespersen T., Nielsen J.B., Liang B., Moller D.V., Hedley P., et al. Mutations in sodium channel beta-subunit SCN3B are associated with early-onset lone atrial fibrillation. Cardiovasc Res Mar 1 2011, 89(4):786-793.
56. Malhotra J.D., Thyagarajan V., Chen C., Isom L.L. Tyrosine-phosphorylated and nonphosphorylated sodium channel beta1 subunits are differentially localized in cardiac myocytes. J Biol Chem Sep 24 2004, 279(39):40748-40754.
57. Hu D., Barajas-Martinez H., Burashnikov E., Springer M., Wu Y., Varro A., et al. A mutation in the beta3 subunit ofthe cardiac sodium channel associated with Brugada ECG phenotype. Circ Cardiovasc Genet 2009, 2(3):270-278.
58. Clatot J., Ziyadeh-Isleem A., Maugenre S., Denjoy I., Liu H., Dilanian G., et al. Dominant-negative effect of SCN5A N-terminal mutations through the interaction of Nav1.5 alpha-subunits. Cardiovasc Res Oct 1 2012, 96(1):53-63.
59. Maier S.K.G., Westenbroek R.E., McCormick K.A., Curtis R., Scheuer T., Catterall W.A. Distinct subcellular localization of different sodium channel alpha and beta subunits in single ventricular myocytes from mouse heart. Circulation Mar 23 2004, 109(11):1421-1427.
60. Wang P., Yang Q., Wu X., Yang Y., Shi L., Wang C., et al. Functional dominant-negative mutation of sodium channel subunit gene SCN3B associated with atrial fibrillation in a Chinese GeneID population. Biochem Biophys Res Commun Jul 16 2010, 398(1):98-104.
61. Kamp T.J. An electrifying iPSC disease model: long QT syndrome type 2 and heart cells in a dish. Cell Stem Cell Feb 4 2011, 8(2):130-131.
62. +) current density, and conduction slowing in desmoglein-2 mutant mice prior to cardiomyopathic changes. Cardiovasc Res Sep 1 2012, 95(4):409-418.
63. Valdivia C.R., Medeiros-Domingo A., Ye B., Shen W.K., Algiers T.J., Ackerman M.J., et al. Loss-of-function mutation of the SCN3B-encoded sodium channel {beta}3 subunit associated with a case of idiopathic ventricular fibrillation. Cardiovasc Res Jun 1 2010, 86(3):392-400.
64. Davis R.P., Casini S., van den Berg C.W., Hoekstra M., Remme C.A., Dambrot C., et al. Cardiomyocytes derived from pluripotent stem cells recapitulate electrophysiological characteristics of an overlap syndrome of cardiac sodium channel disease. Circulation Jun 26 2012, 125(25):3079-3091.
65. Tan B.H., Pundi K.N., Van Norstrand D.W., Valdivia C.R., Tester D.J., Medeiros-Domingo A., et al. Sudden infant death syndrome-associated mutations in the sodium channel beta subunits. Heart Rhythm Jun 2010, 7(6):771-778.
66. Valdivia C.R., Nagatomo T., Makielski J.C. Late Na currents affected by alpha subunit isoform and beta1 subunit co-expression in HEK293 cells. J Mol Cell Cardiol Aug 2002, 34(8):1029-1039.
67. Gavillet B., Rougier J.S., Domenighetti A.A., Behar R., Boixel C., Ruchat P., et al. Cardiac sodium channel Nav1.5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ Res Aug 18 2006, 99(4):407-414.
68. + channel subunits and Ig domains. Nature Sep 26 1996, 383(6598):307-308.
69. Yu F.H., Westenbroek R.E., Silos-Santiago I., McCormick K.A., Lawson D., Ge P., et al. Sodium channel beta 4, a new disulfide-linked auxiliary subunit with similarity to beta 2. J Neurosci Aug 20 2003, 23(20):7577-7585.
70. Albesa M., Ogrodnik J., Rougier J.S., Abriel H. Regulation of the cardiac sodium channel Nav1.5 by utrophin in dystrophin-deficient mice. Cardiovasc Res Feb 1 2011, 89(2):320-328.
71. Remme C.A., Scicluna B.P., Verkerk A.O., Amin A.S., van Brunschot S., Beekman L., et al. Genetically determined differences in sodium current characteristics modulate conduction disease severity in mice with cardiac sodium channelopathy. Circ Res Jun 5 2009, 104(11):1283-1292.
72. + channel expression in Xenopus oocytes by β1 subunits. J Biol Chem Oct 27 1995, 270(43):25696-25701.
73. Qin N., D'Andrea M.R., Lubin M.L., Shafaee N., Codd E.E., Correa A.M. Molecular cloning and functional expression of the human sodium channel beta(1B) subunit, a novel splicing variant of the beta(1) subunit. Eur J Biochem Dec 2003, 270(23):4762-4770.
74. Wang C., Chung B.C., Yan H., Lee S.Y., Pitt G.S. Crystal structure of the ternary complex of a NaV C-terminal domain, a fibroblast growth factor homologous factor, and calmodulin. Structure Jul 3 2012, 20(7):1167-1176.
75. + channels and conduction velocity in murine hearts. Circ Res Sep 16 2011, 109(7):775-782.
76. Vatta M., Ackerman M.J., Ye B., Makielski J.C., Ughanze E.E., Taylor E.W., et al. Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation Nov 14 2006, 114(20):2104-2112.
77. Cheng J., Valdivia C., Vaidyanathn R., Balijepalli R.C., Ackerman M.J., Makielski J.C. Caveolin-3 suppresses late sodium current by inhibiting nNOS-dependent S-nitrosylation of SCN5A. J Mol Cell Cardiol 2013, [Ref Type: Abstract], pii: S0022-2828(13)00094-1.
78. Ou Y.J., Strege P., Miller S.M., Makielski J., Ackerman M., Gibbons S.J., et al. Syntrophin gamma 2 regulates SCN5A gating by a PDZ domain-mediated interaction. J Biol Chem Jan 17 2003, 278(3):1915-1923.
79. Cronk L.B., Ye B., Kaku T., Tester D.J., Vatta M., Makielski J.C., et al. Novel mechanism for sudden infant death syndrome: persistent late sodium current secondary to mutations in caveolin-3. Heart Rhythm Feb 2007, 4(2):161-166.
80. Valdivia C.R., Ueda K., Ackerman M.J., Makielski J.C. GPD1L links redox state to cardiac excitability by PKC-dependent phosphorylation of the sodium channel SCN5A. Am J Physiol Heart Circ Physiol Oct 2009, 297(4):H1446-H1452.
81. Malhotra J.D., Koopmann M.C., Kazen-Gillespie K.A., Fettman N., Hortsch M., Isom L.L. Structural requirements for interaction of sodium channel beta 1 subunits with ankyrin. J Biol Chem Jul 19 2002, 277(29):26681-26688.
82. + current and causes inherited arrhythmias. Circulation Nov 13 2007, 116(20):2260-2268.
83. van Bemmelen M.X., Rougier J.S., Gavillet B., Apotheloz F., Daidie D., Tateyama M., et al. Cardiac voltage-gated sodium channel Nav1.5 is regulated by Nedd4-2 mediated ubiquitination. Circ Res Aug 6 2004, 95(3):284-291.
84. Yarbrough T.L., Lu T., Lee H.C., Shibata E.F. Localization of cardiac sodium channels in caveolin-rich membrane domains: regulation of sodium current amplitude. Circ Res Mar 8 2002, 90(4):443-449.
85. Weiss R., Barmada M.M., Nguyen T., Seibel J.S., Cavlovich D., Kornblit C.A., et al. Clinical and molecular heterogeneity in the Brugada syndrome: a novel gene locus on chromosome 3. Circulation Feb 12 2002, 105(6):707-713.
86. Spampanato J., Kearney J.A., de Haan G., Mcewen D.P., Escayg A., Aradi I., et al. A novel epilepsy mutation in the sodium channel SCN1A identifies a cytoplasmic domain for beta subunit interaction. J Neurosci Nov 3 2004, 24(44):10022-10034.
87. Ueda K., Valdivia C., Medeiros-Domingo A., Tester D.J., Vatta M., Farrugia G., et al. Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci U S A Jul 8 2008, 105(27):9355-9360.
88. Mercier A., Clement R., Harnois T., Bourmeyster N., Faivre J.F., Findlay I., et al. The beta1-subunit of Na(v)1.5 cardiac sodium channel is required for a dominant negative effect through alpha-alpha interaction. PLoS One 2012, 7(11):e48690.
89. Wu L., Yong S.L., Fan C., Ni Y., Yoo S., Zhang T., et al. Identification of a new co-factor, MOG1, required for the full function of cardiac sodium channel Nav 1.5. J Biol Chem Mar 14 2008, 283(11):6968-6978.
90. Sato P.Y., Musa H., Coombs W., Guerrero-Serna G., Patino G.A., Taffet S.M., et al. Loss of plakophilin-2 expression leads to decreased sodium current and slower conduction velocity in cultured cardiac myocytes. Circ Res Sep 11 2009, 105(6):523-526.
91. Malhotra J.D., Chen C., Rivolta I., Abriel H., Malhotra R., Mattei L.N., et al. Characterization of sodium channel α- and β-subunits in rat and mouse cardiac myocytes. Circulation Mar 6 2001, 103(9):1303-1310.
92. Kattygnarath D., Maugenre S., Neyroud N., Balse E., Ichai C., Denjoy I., et al. MOG1: a new susceptibility gene for Brugada syndrome. Circ Cardiovasc Genet Jun 2011, 4(3):261-268.
93. Williams J.C., Armesilla A.L., Mohamed T.M., Hagarty C.L., McIntyre F.H., Schomburg S., et al. The sarcolemmal calcium pump, alpha-1 syntrophin, and neuronal nitric-oxide synthase are parts of a macromolecular protein complex. J Biol Chem Aug 18 2006, 281(33):23341-23348.
94. Van Norstrand D.W., Valdivia C.R., Tester D.J., Ueda K., London B., Makielski J.C., et al. Molecular and functional characterization of novel glycerol-3-phosphate dehydrogenase 1 like gene (GPD1-L) mutations in sudden infant death syndrome. Circulation Nov 13 2007, 116(20):2253-2259.
95. Cheng J., Van Norstrand D.W., Medeiros-Domingo A., Valdivia C., Tan B.H., Ye B., et al. Alpha1-syntrophin mutations identified in sudden infant death syndrome cause an increase in late cardiac sodium current. Circ Arrhythm Electrophysiol Dec 2009, 2(6):667-676.
96. Jespersen T., Gavillet B., van Bemmelen M.X., Cordonier S., Thomas M.A., Staub O., et al. Cardiac sodium channel Na(v)1.5 interacts with and is regulated by the protein tyrosine phosphatase PTPH1. Biochem Biophys Res Commun Oct 6 2006, 348(4):1455-1462.
97. Isom L.L., Ragsdale D.S., De Jongh K.S., Westenbroek R.E., Reber B.F., Scheuer T., et al. Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell Nov 3 1995, 83(3):433-442.
98. Gaborit N., Le Bouter S., Szuts V., Varro A., Escande D., Nattel S., et al. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J Physiol Jul 15 2007, 582(Pt 2):675-693.
99. Xi Y., Ai T., De Lange E., Li Z., Wu G., Brunelli L., et al. Loss of function of hNav1.5 by a ZASP1 mutation associated with intraventricular conduction disturbances in left ventricular noncompaction. Circ Arrhythm Electrophysiol Oct 2012, 5(5):1017-1026.
100. Malhotra J.D., Kazen-Gillespie K., Hortsch M., Isom L.L. Sodium channel beta subunits mediate homophilic cell adhesion and recruit ankyrin to points of cell-cell contact. J Biol Chem Apr 14 2000, 275(15):11383-11388.
101. Bouzidi M., Tricaud N., Giraud P., Kordeli E., Caillol G., Deleuze C., et al. Interaction of the Nav1.2a subunit of the voltage-dependent sodium channel with nodal ankyrinG. In vitro mapping of the interacting domains and association in synaptosomes. J Biol Chem Aug 9 2002, 277(32):28996-29004.
102. Chen C.L., Bharucha V., Chen Y.A., Westenbroek R.E., Brown A., Malhotra J.D., et al. Reduced sodium channel density, altered voltage dependence of inactivation, and increased susceptibility to seizures in mice lacking sodium channel beta 2-subunits. Proc Natl Acad Sci U S A Dec 24 2002, 99(26):17072-17077.
103. Morgan K., Stevens E.B., Shah B., Cox P.J., Dixon A.K., Lee K., et al. Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc Natl Acad Sci U S A Feb 29 2000, 97(5):2308-2313.
104. Hakim P., Brice N., Thresher R., Lawrence J., Zhang Y., Jackson A.P., et al. Scn3b knockout mice exhibit abnormal sino-atrial and cardiac conduction properties. Acta Physiol (Oxf) Oct 1 2009, 198(1):47-59.
105. Valdivia C.R., Medeiros-Domingo A., Ye B., Shen W.K., Algiers T.J., Ackerman M.J., et al. Loss of function mutation of the SCN3B-encoded sodium channel {beta}3 subunit associated with a case of idiopathic ventricular fibrillation. Cardiovasc Res Dec 30 2009, 86(3):392-400.
106. Ko S.H., Lenkowski P.W., Lee H.C., Mounsey J.P., Patel M.K. Modulation of Na(v)1.5 by beta1- and beta3-subunit co-expression in mammalian cells. Pflugers Arch Jan 2005, 449(4):403-412.
107. Hakim P., Gurung I.S., Pedersen T.H., Thresher R., Brice N., Lawrence J., et al. Scn3b knockout mice exhibit abnormal ventricular electrophysiological properties. Prog Biophys Mol Biol Oct 2008, 98(2-3):251-266.
108. Cannon S.C., Bean B.P. Sodium channels gone wild: resurgent current from neuronal and muscle channelopathies. J Clin Invest Jan 2010, 120(1):80-83.
109. Medeiros-Domingo A., Kaku T., Tester D.J., Iturralde-Torres P., Itty A., Ye B., et al. SCN4B-encoded sodium channel {beta}4 subunit in congenital long-QT syndrome. Circulation Jun 25 2007, 116:136-142.
110. Balijepalli R.C., Kamp T.J. Caveolae, ion channels and cardiac arrhythmias. Prog Biophys Mol Biol Oct 2008, 98(2-3):149-160.
111. Sotgia F., Lee J.K., Das K., Bedford M., Petrucci T.C., Macioce P., et al. Caveolin-3 directly interacts with the C-terminal tail of beta-dystroglycan. Identification of a central WW-like domain within caveolin family members. J Biol Chem Dec 1 2000, 275(48):38048-38058.
112. Uittenbogaard A., Smart E.J. Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem Aug 18 2000, 275(33):25595-25599.
113. Rybin V.O., Grabham P.W., Elouardighi H., Steinberg S.F. Caveolae-associated proteins in cardiomyocytes: caveolin-2 expression and interactions with caveolin-3. Am J Physiol Heart Circ Physiol Jul 2003, 285(1):H325-H332.
114. +) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc Natl Acad Sci U S A May 9 2006, 103(19):7500-7505.
115. Ostrom R.S., Bundey R.A., Insel P.A. Nitric oxide inhibition of adenylyl cyclase type 6 activity is dependent upon lipid rafts and caveolin signaling complexes. J Biol Chem May 7 2004, 279(19):19846-19853.
116. Venema V.J., Ju H., Zou R., Venema R.C. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem Nov 7 1997, 272(45):28187-28190.
117. Hayashi T., Arimura T., Ueda K., Shibata H., Hohda S., Takahashi M., et al. Identification and functional analysis of a caveolin-3 mutation associated with familial hypertrophic cardiomyopathy. Biochem Biophys Res Commun Jan 2 2004, 313(1):178-184.
118. Ou X., Ji C., Han X., Zhao X., Li X., Mao Y., et al. Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1). J Mol Biol Mar 31 2006, 357(3):858-869.
119. Strausberg R.L., Feingold E.A., Grouse L.H., Derge J.G., Klausner R.D., Collins F.S., et al. Generation and initial analysis of more than 15,000 full-length human and mouse cDNA sequences. Proc Natl Acad Sci U S A Dec 24 2002, 99(26):16899-16903.
120. Van Norstrand D.W., Valdivia C.R., Tester D.J., Ueda K., London B., Makielski J.C., et al. Molecular and functional characterization of novel glycerol-3-phosphate dehydrogenase 1 like gene (GPD1-L) mutations in sudden infant death syndrome. Circulation Oct 29 2007, 116(20):2253-2259.
121. + channel. Circ Res Mar 1997, 80(3):370-376.
122. + current regulation by pyridine nucleotides. Circ Res Oct 9 2009, 105(8):737-745.
123. Steggerda S.M., Paschal B.M. Identification of a conserved loop in Mog1 that releases GTP from Ran. Traffic Nov 2001, 2(11):804-811.
124. Marfatia K.A., Harreman M.T., Fanara P., Vertino P.M., Corbett A.H. Identification and characterization of the human MOG1 gene. Gene Mar 21 2001, 266(1-2):45-56.
125. Ahn A.H., Freener C.A., Gussoni E., Yoshida M., Ozawa E., Kunkel L.M. The three human syntrophin genes are expressed in diverse tissues, have distinct chromosomal locations, and each bind to dystrophin and its relatives. J Biol Chem Feb 2 1996, 271(5):2724-2730.
126. Oceandy D., Cartwright E.J., Emerson M., Prehar S., Baudoin F.M., Zi M., et al. Neuronal nitric oxide synthase signaling in the heart is regulated by the sarcolemmal calcium pump 4b. Circulation Jan 30 2007, 115(4):483-492.
127. Bennett V., Baines A.J. Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev Jul 2001, 81(3):1353-1392.
128. Cunha S.R., Mohler P.J. Cardiac ankyrins: essential components for development and maintenance of excitable membrane domains in heart. Cardiovasc Res Jul 1 2006, 71(1):22-29.
129. LeMaillet G., Walker B., Lambert S. Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem Jul 25 2003, 278(30):27333-27339.
130. Delva E., Tucker D.K., Kowalczyk A.P. The desmosome. Cold Spring Harb Perspect Biol Aug 2009, 1(2):a002543.
131. Delmar M. Desmosome-ion channel interactions and their possible role in arrhythmogenic cardiomyopathy. Pediatr Cardiol Aug 2012, 33(6):975-979.
132. Cerrone M., Noorman M., Lin X., Chkourko H., Liang F.X., van der N.R., et al. Sodium current deficit and arrhythmogenesis in a murine model of plakophilin-2 haploinsufficiency. Cardiovasc Res Sep 1 2012, 95(4):460-468.
133. Noorman M., Hakim S., Kessler E., Groeneweg J.A., Cox M.G., Asimaki A., et al. Remodeling of the cardiac sodium channel, connexin43, and plakoglobin at the intercalated disk in patients with arrhythmogenic cardiomyopathy. Heart Rhythm Mar 2013, 10(3):412-419.
134. Valdivia C.R., Chu W.W., Pu J.L., Foell J.D., Haworth R.A., Wolff M.R., et al. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. J Mol Cell Cardiol Mar 2005, 38(3):475-483.
135. Lehnart S.E., Ackerman M.J., Benson D.W., Brugada R., Clancy C.E., Donahue J.K., et al. Inherited arrhythmias: a National Heart, Lung, and Blood Institute and Office of Rare Diseases workshop consensus report about the diagnosis, phenotyping, molecular mechanisms, and therapeutic approaches for primary cardiomyopathies of gene mutations affecting ion channel function. Circulation Nov 13 2007, 116(20):2325-2345.