Diseases caused by mutations in Nav1.5 interacting proteins

Cardiac Electrophysiology Clinics

Volumn 6, Issue 4, 2014, Pages 797-809

  Kyle, John W ^a   Makielski, Jonathan C ^a  

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

Author keywords

Arrhythmia; Brugada syndrome; Cardiomyopathy; Late sodium current; Long QT syndrome; Macromolecular complex; SCN5a; Sudden infant death syndrome

Indexed keywords

CAVEOLIN 3; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; PLAKOPHILIN; SODIUM CHANNEL; SODIUM CHANNEL NAV1.5;

BRUGADA SYNDROME; CARDIOMYOPATHY; CONGESTIVE CARDIOMYOPATHY; GENE MUTATION; GENETIC DISORDER; HEART ATRIUM FIBRILLATION; HEART DISEASE; HEART MUSCLE EXCITABILITY; HUMAN; LONG QT SYNDROME; NITROSYLATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SARCOLEMMA; SODIUM CHANNELOPATHY; SODIUM CURRENT; SUDDEN INFANT DEATH SYNDROME; VENTRICULAR NONCOMPACTION;

EID: 84927130987     PISSN: 18779182     EISSN: 18779190     Source Type: Journal    
DOI: 10.1016/j.ccep.2014.08.007     Document Type: Review

References (95)

1. Adsit G.S., Vaidyanathan R., Galler C.M., et al. Channelopathies from mutations in the cardiac sodium channel protein complex. JMol Cell Cardiol 2013, 61:34-43.
2. Abriel H. Cardiac sodium channel Na(v)1.5 and interacting proteins: physiology and pathophysiology. JMol Cell Cardiol 2010, 48(1):2-11.
3. Makielski J.C. Sudden infant death syndrome. Cardiac electrophysiology: from cell to bedside 2014, 975-980. Elsevier, Philadelphia. 6th edition. D.P. Zipes, J. Jalife (Eds.).
4. Isom L.L., De Jongh K.H., Catterall W.A. Auxiliary subunits of voltage-gated ion channels. Neuron 1994, 12:1183-1194.
5. Lin C., Guo X., Lange S., et al. Cypher/ZASP is a novel A-kinase anchoring protein. JBiol Chem 2013, 288(41):29403-29413.
6. Vaidyanathan R., Makielski J.C. Scaffolding proteins and ion channel diseases. Cardiac electrophysiology: from cell to bedside 2014, 229-234. Elsevier, Philadelphia. 6th edition. D.P. Zipes, J. Jalife (Eds.).
7. Murray K.T., Hu N.N., Daw J.R., et al. Functional effects of protein kinase C activation on the human cardiac Na+ channel. Circ Res 1997, 80(3):370-376.
8. van Bemmelen M.X., Rougier J.S., Gavillet B., et al. Cardiac voltage-gated sodium channel Nav1.5 is regulated by Nedd4-2 mediated ubiquitination. Circ Res 2004, 95(3):284-291.
9. Shy D., Gillet L., Abriel H. Cardiac sodium channel NaV1.5 distribution in myocytes via interacting proteins: the multiple pool model. Biochim Biophys Acta 2013, 1833(4):886-894.
10. Petitprez S., Zmoos A.F., Ogrodnik J., et al. SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ Res 2011, 108(3):294-304.
11. Maltsev V.A., Kyle J.W., Mishra S., et al. Molecular identity of the late sodium current in adult dog cardiomyocytes identified by Nav1.5 antisense inhibition. Am J Physiol Heart Circ Physiol 2008, 295(2):H667-H676.
12. London B., Michalec M., Mehdi H., et al. Mutation in glycerol-3-phosphate dehydrogenase 1 like gene (GPD1-L) decreases cardiac Na+ current and causes inherited arrhythmias. Circulation 2007, 116(20):2260-2268.
13. Mazzone A., Strege P.R., Tester D.J., et al. Amutation in telethonin alters nav1.5 function. JBiol Chem 2008, 283(24):16537-16544.
14. Mohler P.J., Rivolta I., Napolitano C., 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 2004, 101(50):17533-17538.
15. Crotti L., Johnson C.N., Graf E., et al. Calmodulin mutations associated with recurrent cardiac arrest in infants. Circulation 2013, 127(9):1009-1017.
16. Bhat H.F., Adams M.E., Khanday F.A. Syntrophin proteins as Santa Claus: role(s) in cell signal transduction. Cell Mol Life Sci 2013, 70(14):2533-2554.
17. Barouch L.A., Harrison R.W., Skaf M.W., et al. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature 2002, 416(6878):337-339.
18. Gavillet B., Rougier J.S., Domenighetti A.A., et al. Cardiac sodium channel Nav1.5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ Res 2006, 99(4):407-414.
19. Ueda K., Valdivia C., Medeiros-Domingo A., et al. Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proc Natl Acad Sci U S A 2008, 105(27):9355-9360.
20. Williams J.C., Armesilla A.L., Mohamed T.M., et al. The sarcolemmal calcium pump, alpha-1 syntrophin, and neuronal nitric-oxide synthase are parts of a macromolecular protein complex. JBiol Chem 2006, 281(33):23341-23348.
21. Oceandy D., Cartwright E.J., Emerson M., et al. Neuronal nitric oxide synthase signaling in the heart is regulated by the sarcolemmal calcium pump 4b. Circulation 2007, 115(4):483-492.
22. Wu G., Ai T., Kim J.J., et al. alpha-1-syntrophin mutation and the long-QT syndrome: a disease of sodium channel disruption. Circ Arrhythm Electrophysiol 2008, 1(3):193-201.
23. Cheng J., Van Norstrand D.W., Medeiros-Domingo A., et al. Alpha1-syntrophin mutations identified in sudden infant death syndrome cause an increase in late cardiac sodium current. Circ Arrhythm Electrophysiol 2009, 2(6):667-676.
24. Hu R.M., Tan B.H., Orland K.M., et al. Digenic inheritance novel mutations in SCN5a and SNTA1 increase late I(Na) contributing to LQT syndrome. Am J Physiol Heart Circ Physiol 2013, 304(7):H994-H1001.
25. Cheng J., Norstrand D.W., Medeiros-Domingo A., et al. LQTS-associated mutation A257G in alpha1-syntrophin interacts with the intragenic variant P74L to modify its biophysical phenotype. Cardiogenetics 2011, 1(10):55-59.
26. Balijepalli R.C., Kamp T.J. Caveolae, ion channels and cardiac arrhythmias. Prog Biophys Mol Biol 2008, 98(2-3):149-160.
27. Li S., Galbiati F., Volonte D., et al. Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes. FEBS Lett 1998, 434(1-2):127-134.
28. McNally E.M., de Sa M.E., Duggan D.J., et al. Caveolin-3 in muscular dystrophy. Hum Mol Genet 1998, 7(5):871-877.
29. Vatta M., Ackerman M.J., Ye B., et al. Mutant caveolin-3 induces persistent late sodium current and is associated with long-QT syndrome. Circulation 2006, 114(20):2104-2112.
30. Cronk L.B., Ye B., Kaku T., et al. Novel mechanism for sudden infant death syndrome: persistent late sodium current secondary to mutations in caveolin-3. Heart Rhythm 2007, 4(2):161-166.
31. Venema V.J., Ju H., Zou R., et al. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. JBiol Chem 1997, 272(45):28187-28190.
32. Cheng J., Valdivia C.R., Vaidyanathan R., et al. Caveolin-3 suppresses late sodium current by inhibiting nNOS-dependent S-nitrosylation of SCN5A. JMol Cell Cardiol 2013, 61:102-110.
33. Vaidyanathan R., Vega A.L., Song C., et al. The interaction of caveolin 3 with the inward rectifier channel Kir2.1; physiology and pathology related to LQT9. JBiol Chem 2013, 288(24):17472-17480.
34. Ou X., Ji C., Han X., et al. Crystal structures of human glycerol 3-phosphate dehydrogenase 1 (GPD1). JMol Biol 2006, 357(3):858-869.
35. Weiss R., Barmada M.M., Nguyen T., et al. Clinical and molecular heterogeneity in the Brugada syndrome: a novel gene locus on chromosome 3. Circulation 2002, 105(6):707-713.
36. Van Norstrand D.W., Valdivia C.R., Tester D.J., et al. Molecular and functional characterization of novel glycerol-3-phosphate dehydrogenase 1 like gene (GPD1-L) mutations in sudden infant death syndrome. Circulation 2007, 116(20):2253-2259.
37. Valdivia C.R., Ueda K., Ackerman M.J., et al. GPD1L links redox state to cardiac excitability by PKC-dependent phosphorylation of the sodium channel SCN5A. Am J Physiol Heart Circ Physiol 2009, 297(4):H1446-H1452.
38. Liu M., Sanyal S., Gao G., et al. Cardiac Na+ current regulation by pyridine nucleotides. Circ Res 2009, 105(8):737-745.
39. Liu M., Liu H., Dudley S.C. Reactive oxygen species originating from mitochondria regulate the cardiac sodium channel. Circ Res 2010, 107(8):967-974.
40. Makiyama T., Akao M., Haruna Y., et al. Mutation analysis of the glycerol-3 phosphate dehydrogenase-1 like (GPD1L) gene in Japanese patients with Brugada syndrome. Circ J 2008, 72(10):1705-1706.
41. Westaway S.K., Reinier K., Huertas-Vazquez A., et al. Common variants in CASQ2, GPD1L, and NOS1AP are significantly associated with risk of sudden death in patients with coronary artery disease. Circ Cardiovasc Genet 2011, 4(4):397-402.
42. Steggerda S.M., Paschal B.M. Identification of a conserved loop in Mog1 that releases GTP from Ran. Traffic 2001, 2(11):804-811.
43. Marfatia K.A., Harreman M.T., Fanara P., et al. Identification and characterization of the human MOG1 gene. Gene 2001, 266(1-2):45-56.
44. Wu L., Yong S.L., Fan C., et al. Identification of a new co-factor, MOG1, required for the full function of cardiac sodium channel Nav 1.5. JBiol Chem 2008, 283(11):6968-6978.
45. Chakrabarti S., Wu X., Yang Z., et al. MOG1 rescues defective trafficking of Na(v)1.5 mutations in Brugada syndrome and sick sinus syndrome. Circ Arrhythm Electrophysiol 2013, 6(2):392-401.
46. Kattygnarath D., Maugenre S., Neyroud N., et al. MOG1: a new susceptibility gene for Brugada syndrome. Circ Cardiovasc Genet 2011, 4(3):261-268.
47. Olesen M.S., Jensen N.F., Holst A.G., et al. Anovel nonsense variant in Nav1.5 cofactor MOG1 eliminates its sodium current increasing effect and may increase the risk of arrhythmias. Can J Cardiol 2011, 27(4):523.
48. Campuzano O., Berne P., Selga E., et al. Brugada syndrome and p.E61X_RANGRF. Cardiol J 2014, 21(2):121-127.
49. Bass-Zubek A.E., Godsel L.M., Delmar M., et al. Plakophilins: multifunctional scaffolds for adhesion and signaling. Curr Opin Cell Biol 2009, 21(5):708-716.
50. Kowalczyk A.P., Green K.J. Structure, function, and regulation of desmosomes. Prog Mol Biol Transl Sci 2013, 116:95-118.
51. van Tintelen J.P., Entius M.M., Bhuiyan Z.A., et al. Plakophilin-2 mutations are the major determinant of familial arrhythmogenic right ventricular dysplasia/cardiomyopathy. Circulation 2006, 113(13):1650-1658.
52. Valdivia C.R., Chu W.W., Pu J.L., et al. Increased late sodium current in myocytes from a canine heart failure model and from failing human heart. JMol Cell Cardiol 2005, 38(3):475-483.
53. Noorman M., Hakim S., Kessler E., et al. Remodeling of the cardiac sodium channel, connexin43, and plakoglobin at the intercalated disk in patients with arrhythmogenic cardiomyopathy. Heart Rhythm 2013, 10(3):412-419.
54. Sato P.Y., Musa H., Coombs W., et al. Loss of plakophilin-2 expression leads to decreased sodium current and slower conduction velocity in cultured cardiac myocytes. Circ Res 2009, 105(6):523-526.
55. Cerrone M., Noorman M., Lin X., et al. Sodium current deficit and arrhythmogenesis in a murine model of plakophilin-2 haploinsufficiency. Cardiovasc Res 2012, 95(4):460-468.
56. Cerrone M., Lin X., Zhang M., et al. Missense mutations in plakophilin-2 cause sodium current deficit and associate with a Brugada syndrome phenotype. Circulation 2014, 129(10):1092-1103.
57. Cerrone M., Delmar M. Desmosomes and the sodium channel complex: Implications for arrhythmogenic cardiomyopathy and Brugada syndrome. Trends Cardiovasc Med 2014, 24(5):184-190.
58. Wielowieyski P.A., Sevinc S., Guzzo R., et al. Alternative splicing, expression, and genomic structure ofthe 3' region of the gene encoding the sarcolemmal-associated proteins (SLAPs) defines a novel class of coiled-coil tail-anchored membrane proteins. JBiol Chem 2000, 275(49):38474-38481.
59. Ishikawa T., Sato A., Marcou C.A., et al. Anovel disease gene for Brugada syndrome: sarcolemmal membrane-associated protein gene mutations impair intracellular trafficking of hNav1.5. Circ Arrhythm Electrophysiol 2012, 5(6):1098-1107.
60. te Velthuis A.J., Isogai T., Gerrits L., et al. Insights into the molecular evolution of the PDZ/LIM family and identification of a novel conserved protein motif. PLoS One 2007, 2(2):e189.
61. Vatta M., Mohapatra B., Jimenez S., et al. Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. JAm Coll Cardiol 2003, 42(11):2014-2027.
62. Zheng M., Cheng H., Banerjee I., et al. ALP/Enigma PDZ-LIM domain proteins in the heart. JMol Cell Biol 2010, 2(2):96-102.
63. Xi Y., Ai T., De Lange E., et al. Loss of function of hNav1.5 by a ZASP1 mutation associated with intraventricular conduction disturbances in left ventricular noncompaction. Circ Arrhythm Electrophysiol 2012, 5(5):1017-1026.
64. Allouis M., Le Bouffant F., Wilders R., et al. 14-3-3 is a regulator of the cardiac voltage-gated sodium channel Nav1.5. Circ Res 2006, 98(12):1538-1546.
65. Ziane R., Huang H., Moghadaszadeh B., et al. Cell membrane expression of cardiac sodium channel Na(v)1.5 is modulated by alpha-actinin-2 interaction. Biochemistry 2010, 49(1):166-178.
66. Mohler P.J., Wehrens X.H. Mechanisms of human arrhythmia syndromes: abnormal cardiac macromolecular interactions. Physiology (Bethesda) 2007, 22:342-350.
67. Lowe J.S., Palygin O., Bhasin N., et al. Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. JCell Biol 2008, 180(1):173-186.
68. Dhar Malhotra J., Chen C., Rivolta I., et al. Characterization of sodium channel alpha- and beta-subunits in rat and mouse cardiac myocytes. Circulation 2001, 103(9):1303-1310.
69. 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 2002, 34(8):1029-1039.
70. Maltsev V.A., Kyle J.W., Undrovinas A. Late Na+ current produced by human cardiac Na+ channel isoform Nav1.5 is modulated by its beta1 subunit. JPhysiol Sci 2009, 59(3):217-225.
71. Herfst L.J., Potet F., Bezzina C.R., et al. Na+ channel mutation leading to loss of function and non-progressive cardiac conduction defects. JMol Cell Cardiol 2003, 35(5):549-557.
72. Nuss H.B., Chiamvimonvat N., Perez-Garcia M.T., et al. Functional association of the β1 subunit with human cardiac (hH1) and rat skeletal muscle (μ1) sodium channel α subunits expressed in Xenopus oocytes. JGen Physiol 1995, 106(6):1171-1191.
73. Lopez-Santiago L.F., Meadows L.S., Ernst S.J., et al. Sodium channel Scn1b null mice exhibit prolonged QT and RR intervals. JMol Cell Cardiol 2007, 43(5):636-647.
74. Johnson D., Bennett E.S. Isoform-specific effects of the beta2 subunit on voltage-gated sodium channel gating. JBiol Chem 2006, 281(36):25875-25881.
75. Mishra S., Undrovinas N.A., Maltsev V.A., et al. 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 2011, 301(4):H1596-H1605.
76. Hakim P., Brice N., Thresher R., et al. Scn3b knockout mice exhibit abnormal sino-atrial and cardiac conduction properties. Acta Physiol (Oxf) 2010, 198(1):47-59.
77. Fahmi A.I., Patel M., Stevens E.B., et al. The sodium channel beta-subunit SCN3b modulates the kinetics of SCN5a and is expressed heterogeneously in sheep heart. JPhysiol 2001, 537(Pt 3):693-700.
78. Hakim P., Gurung I.S., Pedersen T.H., et al. Scn3b knockout mice exhibit abnormal ventricular electrophysiological properties. Prog Biophys Mol Biol 2008, 98(2-3):251-266.
79. Medeiros-Domingo A., Kaku T., Tester D.J., et al. SCN4B-encoded sodium channel {beta}4 subunit in congenital long-QT syndrome. Circulation 2007, 116:136-142.
80. Remme C.A., Scicluna B.P., Verkerk A.O., et al. Genetically determined differences in sodium current characteristics modulate conduction disease severity in mice with cardiac sodium channelopathy. Circ Res 2009, 104(11):1283-1292.
81. Hund T.J., Koval O.M., Li J., et al. Abeta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. JClin Invest 2010, 120(10):3508-3519.
82. Kim J., Ghosh S., Liu H., et al. Calmodulin mediates Ca2+ sensitivity of sodium channels. JBiol Chem 2004, 279(43):45004-45012.
83. Chagot B., Chazin W.J. Solution NMR structure of Apo-calmodulin in complex with the IQ motif of human cardiac sodium channel NaV1.5. JMol Biol 2011, 406(1):106-119.
84. Tan H.L., Kupershmidt S., Zhang R., et al. Acalcium sensor in the sodium channel modulates cardiac excitability. Nature 2002, 415(6870):442-447.
85. Aiba T., Hesketh G.G., Liu T., et al. Na+ channel regulation by Ca2+/calmodulin and Ca2+/calmodulin-dependent protein kinase II in guinea-pig ventricular myocytes. Cardiovasc Res 2010, 85(3):454-463.
86. Koval O.M., Snyder J.S., Wolf R.M., et al. Ca2+/calmodulin-dependent protein kinase II-based regulation of voltage-gated Na+ channel in cardiac disease. Circulation 2012, 126(17):2084-2094.
87. 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 2002, 54(2):270-279.
88. Malhotra J.D., Thyagarajan V., Chen C., et al. Tyrosine-phosphorylated and nonphosphorylated sodium channel beta1 subunits are differentially localized in cardiac myocytes. JBiol Chem 2004, 279(39):40748-40754.
89. Jansen J.A., Noorman M., Musa H., 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 2012, 9(4):600-607.
90. Rizzo S., Lodder E.M., Verkerk A.O., et al. Intercalated disc abnormalities, reduced Na(+) current density, and conduction slowing in desmoglein-2 mutant mice prior to cardiomyopathic changes. Cardiovasc Res 2012, 95(4):409-418.
91. Albesa M., Ogrodnik J., Rougier J.S., et al. Regulation of the cardiac sodium channel Nav1.5 by utrophin in dystrophin-deficient mice. Cardiovasc Res 2011, 89(2):320-328.
92. Wang C., Hennessey J.A., Kirkton R.D., et al. Fibroblast growth factor homologous factor 13 regulates Na+ channels and conduction velocity in murine hearts. Circ Res 2011, 109(7):775-782.
93. Ou Y.J., Strege P., Miller S.M., et al. Syntrophin gamma 2 regulates SCN5A Gating by a PDZ domain-mediated interaction. JBiol Chem 2003, 278(3):1915-1923.
94. Jespersen T., Gavillet B., van Bemmelen M.X., et al. Cardiac sodium channel Na(v)1.5 interacts with and is regulated by the protein tyrosine phosphatase PTPH1. Biochem Biophys Res Commun 2006, 348(4):1455-1462.
95. Trane A.E., Pavlov D., Sharma A., et al. Deciphering the binding of caveolin-1 to client protein endothelial nitric oxide synthase (eNOS): scaffolding sub-domain identification, interaction modeling, and biological significance. JBiol Chem 2014, 289(19):13273-13283.