Expression of the sialyltransferase, ST3Gal4, impacts cardiac voltage-gated sodium channel activity, refractory period and ventricular conduction

Journal of Molecular and Cellular Cardiology

Volumn 59, Issue , 2013, Pages 117-127

  Ednie, Andrew R ^a   Horton, Kofi Kermit ^a   Wu, Jiashin ^a   Bennett, Eric S ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Action potential; Arrhythmias; Congenital disorders of glycosylation; Glycosylation; Ion channels; Sialic acids

Indexed keywords

GLYCOPROTEIN; VOLTAGE GATED SODIUM CHANNEL; BETA GALACTOSIDE ALPHA 2,3 SIALYLTRANSFERASE; BETA-GALACTOSIDE ALPHA-2,3-SIALYLTRANSFERASE; SIALYLTRANSFERASE;

ACTION POTENTIAL; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CHANNEL GATING; CONTROLLED STUDY; GENE; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; HEART DEPOLARIZATION; HEART MUSCLE REFRACTORY PERIOD; HEART VENTRICLE CONDUCTION; MALE; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; SIALYLATION; SODIUM CURRENT; ST3GAL4 GENE; WHOLE CELL PATCH CLAMP; ANIMAL; CELL CULTURE; ELECTROPHYSIOLOGY; ENZYMOLOGY; GENETICS; GLYCOSYLATION; HEART MUSCLE CELL; HEART VENTRICLE; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; ELECTROPHYSIOLOGY; GLYCOSYLATION; HEART VENTRICLES; MALE; MICE; MICE, TRANSGENIC; MYOCYTES, CARDIAC; SIALYLTRANSFERASES; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84875359727     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.02.013     Document Type: Article

References (57)

1. Schroeter, A., Walzik, S., Blechschmidt, S., Haufe, V., Benndorf, K., Zimmer, T., Structure and function of splice variants of the cardiac voltage-gated sodium channel Na(v)1.5. J Mol Cell Cardiol 49 (2010), 16–24.
2. Remme, C.A., Bezzina, C.R., Sodium channel (dys)function and cardiac arrhythmias. Cardiovasc Ther 28 (2010), 287–294.
3. Andavan, G.S., Lemmens-Gruber, R., Voltage-gated sodium channels: mutations, channelopathies and targets. Curr Med Chem 18 (2011), 377–397.
4. Schmidt, J.W., Catterall, W.A., Palmitylation, sulfation, and glycosylation of the alpha subunit of the sodium channel. Role of post-translational modifications in channel assembly. J Biol Chem 262 (1987), 13713–13723.
5. Montpetit, M.L., Stocker, P.J., Schwetz, T.A., Harper, J.M., Norring, S.A., Schaffer, L., et al. Regulated and aberrant glycosylation modulate cardiac electrical signaling. Proc Natl Acad Sci U S A 106 (2009), 16517–16522.
6. Ednie, A.R., Bennett, E.S., Modulation of voltage-gated ion channels by sialylation. Comprehensive physiology, 2011, John Wiley & Sons, Inc.
7. Tyrrell, L., Renganathan, M., Dib-Hajj, S.D., Waxman, S.G., Glycosylation alters steady-state inactivation of sodium channel Nav1.9/NaN in dorsal root ganglion neurons and is developmentally regulated. J Neurosci 21 (2001), 9629–9637.
8. Stocker, P.J., Bennett, E.S., Differential sialylation modulates voltage-gated Na + channel gating throughout the developing myocardium. J Gen Physiol 127 (2006), 253–265.
9. Jaeken, J., Congenital disorders of glycosylation. Ann N Y Acad Sci 1214 (2010), 190–198.
10. Footitt, E.J., Karimova, A., Burch, M., Yayeh, T., Dupre, T., Vuillaumier-Barrot, S., et al. Cardiomyopathy in the congenital disorders of glycosylation (CDG): a case of late presentation and literature review. J Inherit Metab Dis 32:Suppl (2009), S313–S319.
11. Freeze, H.H., Eklund, E.A., Ng, B.G., Patterson, M.C., Neurology of inherited glycosylation disorders. Lancet Neurol 11 (2012), 453–466.
12. Sparks, S.E., Krasnewich, D.M., Congenital disorders of glycosylation overview. 1993.
13. Freeze, H.H., Aebi, M., Altered glycan structures: the molecular basis of congenital disorders of glycosylation. Curr Opin Struct Biol 15 (2005), 490–498.
14. Waite, A., Tinsley, C.L., Locke, M., Blake, D.J., The neurobiology of the dystrophin-associated glycoprotein complex. Ann Med 41 (2009), 344–359.
15. Gehrmann, J., Sohlbach, K., Linnebank, M., Bohles, H.J., Buderus, S., Kehl, H.G., et al. Cardiomyopathy in congenital disorders of glycosylation. Cardiol Young 13 (2003), 345–351.
16. Al-Owain, M., Mohamed, S., Kaya, N., Zagal, A., Matthijs, G., Jaeken, J., A novel mutation and first report of dilated cardiomyopathy in ALG6-CDG (CDG-Ic): a case report. Orphanet J Rare Dis, 5, 2010, 7.
17. Kranz, C., Basinger, A.A., Gucsavas-Calikoglu, M., Sun, L., Powell, C.M., Henderson, F.W., et al. Expanding spectrum of congenital disorder of glycosylation Ig (CDG-Ig): sibs with a unique skeletal dysplasia, hypogammaglobulinemia, cardiomyopathy, genital malformations, and early lethality. Am J Med Genet A 143A (2007), 1371–1378.
18. Ufret-Vincenty, C.A., Baro, D.J., Lederer, W.J., Rockman, H.A., Quinones, L.E., Santana, L.F., Role of sodium channel deglycosylation in the genesis of cardiac arrhythmias in heart failure. J Biol Chem 276 (2001), 28197–28203.
19. Libby, P., Alroy, J., Pereira, M.E., A neuraminidase from Trypanosoma cruzi removes sialic acid from the surface of mammalian myocardial and endothelial cells. J Clin Invest 77 (1986), 127–135.
20. Yacoub, S., Mocumbi, A.O., Yacoub, M.H., Neglected tropical cardiomyopathies: I. Chagas disease: myocardial disease. Heart 94 (2008), 244–248.
21. Kiarash, A., Kelly, C.E., Phinney, B.S., Valdivia, H.H., Abrams, J., Cala, S.E., Defective glycosylation of calsequestrin in heart failure. Cardiovasc Res 63 (2004), 264–272.
22. Takashima, S., Characterization of mouse sialyltransferase genes: their evolution and diversity. Biosci Biotechnol Biochem 72 (2008), 1155–1167.
23. Ellies, L.G., Ditto, D., Levy, G.G., Wahrenbrock, M., Ginsburg, D., Varki, A., et al. Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands. Proc Natl Acad Sci U S A 99 (2002), 10042–10047.
24. Ellies, L.G., Sperandio, M., Underhill, G.H., Yousif, J., Smith, M., Priatel, J.J., et al. Sialyltransferase specificity in selectin ligand formation. Blood 100 (2002), 3618–3625.
25. Grewal, P.K., Uchiyama, S., Ditto, D., Varki, N., Le, D.T., Nizet, V., et al. The Ashwell receptor mitigates the lethal coagulopathy of sepsis. Nat Med 14 (2008), 648–655.
26. Sperandio, M., Frommhold, D., Babushkina, I., Ellies, L.G., Olson, T.S., Smith, M.L., et al. Alpha 2,3-sialyltransferase-IV is essential for L-selectin ligand function in inflammation. Eur J Immunol 36 (2006), 3207–3215.
27. Brouillette, J., Clark, R.B., Giles, W.R., Fiset, C., Functional properties of K + currents in adult mouse ventricular myocytes. J Physiol 559 (2004), 777–798.
28. Barry, D.M., Trimmer, J.S., Merlie, J.P., Nerbonne, J.M., Differential expression of voltage-gated K + channel subunits in adult rat heart. Relation to functional K + channels?. Circ Res 77 (1995), 361–369.
29. Bennett, E.S., Effects of channel cytoplasmic regions on the activation mechanisms of cardiac versus skeletal muscle Na(+) channels. Biophys J 77 (1999), 2999–3009.
30. Morita, H., Zipes, D.P., Morita, S.T., Wu, J., Genotype-phenotype correlation in tissue models of Brugada syndrome simulating patients with sodium and calcium channelopathies. Heart Rhythm 7 (2010), 820–827.
31. Ueda, N., Zipes, D.P., Wu, J., Coronary occlusion and reperfusion promote early after depolarizations and ventricular tachycardia in a canine tissue model of type 3 long QT syndrome. Am J Physiol Heart Circ Physiol 290 (2006), H607–H612.
32. Morita, S.T., Zipes, D.P., Morita, H., Wu, J., Analysis of action potentials in the canine ventricular septum: no phenotypic expression of M cells. Cardiovasc Res 74 (2007), 96–103.
33. Chen, Q., Kirsch, G.E., Zhang, D., Brugada, R., Brugada, J., Brugada, P., et al. Genetic basis and molecular mechanism for idiopathic ventricular fibrillation. Nature 392 (1998), 293–296.
34. Haufe, V., Camacho, J.A., Dumaine, R., Gunther, B., Bollensdorff, C., von Banchet, G.S., et al. Expression pattern of neuronal and skeletal muscle voltage-gated Na + channels in the developing mouse heart. J Physiol 564 (2005), 683–696.
35. Maier, S.K., 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 109 (2004), 1421–1427.
36. Catterall, W.A., Goldin, A.L., Waxman, S.G., International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57 (2005), 397–409.
37. Rosker, C., Lohberger, B., Hofer, D., Steinecker, B., Quasthoff, S., Schreibmayer, W., The TTX metabolite 4,9-anhydro-TTX is a highly specific blocker of the Na(v1.6) voltage-dependent sodium channel. Am J Physiol Cell Physiol 293 (2007), C783–C789.
38. Abriel, H., Cabo, C., Wehrens, X.H., Rivolta, I., Motoike, H.K., Memmi, M., et al. Novel arrhythmogenic mechanism revealed by a long-QT syndrome mutation in the cardiac Na(+) channel. Circ Res 88 (2001), 740–745.
39. Amin, A.S., Asghari-Roodsari, A., Tan, H.L., Cardiac sodium channelopathies. Pflugers Arch 460 (2010), 223–237.
40. Jones, D.K., Ruben, P.C., Biophysical defects in voltage.gated sodium channels associated with long QT and Brugada syndromes. Channels (Austin) 2 (2008), 70–80.
41. Wang, D.W., Yazawa, K., George, A.L. Jr., Bennett, P.B., Characterization of human cardiac Na + channel mutations in the congenital long QT syndrome. Proc Natl Acad Sci U S A 93 (1996), 13200–13205.
42. Johnson, D., Bennett, E.S., Isoform-specific effects of the beta2 subunit on voltage-gated sodium channel gating. J Biol Chem 281 (2006), 25875–25881.
43. Johnson, D., Montpetit, M.L., Stocker, P.J., Bennett, E.S., The sialic acid component of the beta1 subunit modulates voltage-gated sodium channel function. J Biol Chem 279 (2004), 44303–44310.
44. Bennett, E.S., Isoform-specific effects of sialic acid on voltage-dependent Na + channel gating: functional sialic acids are localized to the S5–S6 loop of domain I. J Physiol 538 (2002), 675–690.
45. Isaev, D., Isaeva, E., Shatskih, T., Zhao, Q., Smits, N.C., Shworak, N.W., et al. Role of extracellular sialic acid in regulation of neuronal and network excitability in the rat hippocampus. J Neurosci 27 (2007), 11587–11594.
46. Brunet, S., Aimond, F., Li, H., Guo, W., Eldstrom, J., Fedida, D., et al. Heterogeneous expression of repolarizing, voltage-gated K + currents in adult mouse ventricles. J Physiol 559 (2004), 103–120.
47. Martin, P.T., Freeze, H.H., Glycobiology of neuromuscular disorders. Glycobiology 13 (2003), 67R–75R.
48. Pearl, P.L., Krasnewich, D., Neurologic course of congenital disorders of glycosylation. J Child Neurol 16 (2001), 409–413.
49. Mucci, J., Hidalgo, A., Mocetti, E., Argibay, P.F., Leguizamon, M.S., Campetella, O., Thymocyte depletion in Trypanosoma cruzi infection is mediated by trans-sialidase-induced apoptosis on nurse cells complex. Proc Natl Acad Sci U S A 99 (2002), 3896–3901.
50. Bustamante, J.M., Rivarola, H.W., Fretes, R., Paglini-Oliva, P.A., Weekly electrocardiographic pattern in mice infected with two different Trypanosoma cruzi strains. Int J Cardiol 102 (2005), 211–217.
51. Ohtsubo, K., Takamatsu, S., Minowa, M.T., Yoshida, A., Takeuchi, M., Marth, J.D., Dietary and genetic control of glucose transporter 2 glycosylation promotes insulin secretion in suppressing diabetes. Cell 123 (2005), 1307–1321.
52. Xu, J., Zhou, Q., Xu, W., Cai, L., Endoplasmic reticulum stress and diabetic cardiomyopathy. Exp Diabetes Res, 2012, 2012, 827971.
53. Groenendyk, J., Agellon, L.B., Michalak, M., Coping with endoplasmic reticulum stress in the cardiovascular system. Annu Rev Physiol 75 (2013), 49–67.
54. Aiba, T., Tomaselli, G.F., Electrical remodeling in the failing heart. Curr Opin Cardiol 25 (2010), 29–36.
55. Casis, O., Echevarria, E., Diabetic cardiomyopathy: electromechanical cellular alterations. Curr Vasc Pharmacol 2 (2004), 237–248.
56. Zhang, Z.S., Tranquillo, J., Neplioueva, V., Bursac, N., Grant, A.O., Sodium channel kinetic changes that produce Brugada syndrome or progressive cardiac conduction system disease. Am J Physiol Heart Circ Physiol 292 (2007), H399–H407.
57. Terrenoire, C., Simhaee, D., Kass, R.S., Role of sodium channels in propagation in heart muscle: how subtle genetic alterations result in major arrhythmic disorders. J Cardiovasc Electrophysiol 18 (2007), 900–905.