Prolongation of Action Potential Duration and QT Interval during Epilepsy Linked to Increased Contribution of Neuronal Sodium Channels to Cardiac Late Na + Current

Circulation: Arrhythmia and Electrophysiology

Volumn 8, Issue 4, 2015, Pages 912-920

  Biet, Michael ^a   Morin, Nathalie ^a   Lessard Beaudoin, Melissa ^a   Graham, Rona K ^a   Duss, Sandra ^b   Gagné, Jonathan ^b   Sanon, Nathalie T ^b   Carmant, Lionel ^b   Dumaine, Robert ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

Author keywords

action potentials; arrhythmias; cardiac; death; electrophysiology; epilepsy; sodium channels; sudden

Indexed keywords

SODIUM CHANNEL; SODIUM CHANNEL NAV1.1; SODIUM CHANNEL NAV1.5; TETRODOTOXIN; DNA;

ACTION POTENTIAL DURATION; ADULT; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EPILEPSY; HEART ARRHYTHMIA; HEART CONDUCTION; HEART MUSCLE CELL; HEART MUSCLE EXCITABILITY; HEART REPOLARIZATION; MALE; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QT PROLONGATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SODIUM CURRENT; SUDDEN DEATH; VOLTAGE CLAMP TECHNIQUE; WESTERN BLOTTING; ACTION POTENTIAL; ANIMAL; BIOSYNTHESIS; COMPLICATION; ETIOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MORTALITY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ARRHYTHMIAS, CARDIAC; BLOTTING, WESTERN; DEATH, SUDDEN; DNA; EPILEPSY; GENE EXPRESSION REGULATION; MALE; MYOCYTES, CARDIAC; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; PATCH-CLAMP TECHNIQUES; RATS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84939785019     PISSN: 19413149     EISSN: 19413084     Source Type: Journal    
DOI: 10.1161/CIRCEP.114.002693     Document Type: Article

References (50)

1. Logroscino G, Hesdorffer DC, Cascino G, Hauser WA, Coeytaux A, Galobardes B, Morabia A, Jallon P. Mortality after a first episode of status epilepticus in the United States and Europe. Epilepsia. 2005; 46 Suppl 11: 46-48. doi: 10. 1111/j. 1528-1167. 2005. 00409. x.
2. Opherk C, Coromilas J, Hirsch LJ. Heart rate and EKG changes in 102 seizures: Analysis of influencing factors. Epilepsy Res. 2002; 52: 117-127.
3. Nei M, Ho RT, Sperling MR. EKG abnormalities during partial seizures in refractory epilepsy. Epilepsia. 2000; 41: 542-548.
4. Nei M, Ho RT, Abou-Khalil BW, Drislane FW, Liporace J, Romeo A, Sperling MR. EEG and ECG in sudden unexplained death in epilepsy. Epilepsia. 2004; 45: 338-345. doi: 10. 1111/j. 0013-9580. 2004. 05503. x.
5. Tigaran S, Mølgaard H, Dam M. Atrio-ventricular block: A possible explanation of sudden unexpected death in epilepsy. Acta Neurol Scand. 2002; 106: 229-233.
6. Dasheiff RM, Dickinson LJ. Sudden unexpected death of epileptic patient due to cardiac arrhythmia after seizure. Arch Neurol. 1986; 43: 194-196.
7. Dasheiff RM. Sudden unexpected death in epilepsy: A series from an epilepsy surgery program and speculation on the relationship to sudden cardiac death. J Clin Neurophysiol. 1991; 8: 216-222.
8. Metcalf CS, Poelzing S, Little JG, Bealer SL. Status epilepticus induces cardiac myofilament damage and increased susceptibility to arrhythmias in rats. Am J Physiol Heart Circ Physiol. 2009; 297: H2120-H2127. doi: 10. 1152/ajpheart. 00724. 2009.
9. Bealer SL, Little JG. Seizures following hippocampal kindling induce QT interval prolongation and increased susceptibility to arrhythmias in rats. Epilepsy Res. 2013; 105: 216-219. doi: 10. 1016/j. eplepsyres. 2013. 01. 002.
10. Dumaine R, Wang Q, Keating MT, Hartmann HA, Schwartz PJ, Brown AM, Kirsch GE. Multiple mechanisms of Na+ channel-linked long-QT syndrome. Circ Res. 1996; 78: 916-924.
11. Dumaine R, Kirsch GE. Mechanism of lidocaine block of late current in long Q-T mutant Na+ channels. Am J Physiol. 1998; 274(2 pt 2): H477-H487.
12. Brugada R, Hong K, Cordeiro JM, Dumaine R. Short QT syndrome. CMAJ. 2005; 173: 1349-1354. doi: 10. 1503/cmaj. 050596.
13. Moreno JD, Clancy CE. Pathophysiology of the cardiac late Na current and its potential as a drug target. J Mol Cell Cardiol. 2012; 52: 608-619. doi: 10. 1016/j. yjmcc. 2011. 12. 003.
14. Chaitman BR. Ranolazine for the treatment of chronic angina and potential use in other cardiovascular conditions. Circulation. 2006; 113: 2462-2472. doi: 10. 1161/CIRCULATIONAHA. 105. 597500.
15. Zygmunt AC, Nesterenko VV, Rajamani S, Hu D, Barajas-Martinez H, Belardinelli L, Antzelevitch C. Mechanisms of atrial-selective block of Na+ channels by ranolazine: I. Experimental analysis of the usedependent block. Am J Physiol Heart Circ Physiol. 2011; 301: H1606-H1614. doi: 10. 1152/ajpheart. 00242. 2011.
16. Carmeliet E. Slow inactivation of the sodium current in rabbit cardiac Purkinje fibres. Pflugers Arch. 1987; 408: 18-26.
17. Guo F, Yu N, Cai JQ, Quinn T, Zong ZH, Zeng YJ, Hao LY. Voltagegated sodium channel Nav1. 1, Nav1. 3 and beta1 subunit were up-regulated in the hippocampus of spontaneously epileptic rat. Brain Res Bull. 2008; 75: 179-187. doi: 10. 1016/j. brainresbull. 2007. 10. 005.
18. Guo F, Xu X, Cai J, Hu H, Sun W, He G, Shao D, Wang L, Chen T, Shaw C, Zhu T, Hao L. The up-regulation of voltage-gated sodium channels subtypes coincides with an increased sodium current in hippocampal neuronal culture model. Neurochem Int. 2013; 62: 287-295. doi: 10. 1016/j. neuint. 2013. 01. 005.
19. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr. Molecular basis of an inherited epilepsy. Neuron. 2002; 34: 877-884.
20. Sugawara T, Mazaki-Miyazaki E, Ito M, Nagafuji H, Fukuma G, Mitsudome A, Wada K, Kaneko S, Hirose S, Yamakawa K. Nav1. 1 mutations cause febrile seizures associated with afebrile partial seizures. Neurology. 2001; 57: 703-705.
21. Sugawara T, Tsurubuchi Y, Agarwala KL, Ito M, Fukuma G, Mazaki-Miyazaki E, Nagafuji H, Noda M, Imoto K, Wada K, Mitsudome A, Kaneko S, Montal M, Nagata K, Hirose S, Yamakawa K. A missense mutation of the Na+ channel alpha II subunit gene Na(v)1. 2 in a patient with febrile and afebrile seizures causes channel dysfunction. Proc Natl Acad Sci U S A. 2001; 98: 6384-6389. doi: 10. 1073/pnas. 111065098.
22. Christidis D, Kalogerakis D, Chan TY, Mauri D, Alexiou G, Terzoudi A. Is primidone the drug of choice for epileptic patients with QT-prolongation? A comprehensive analysis of literature. Seizure. 2006; 15: 64-66. doi: 10. 1016/ j. seizure. 2005. 10. 002.
23. Akalin F, Tirtir A, Yilmaz Y. Increased QT dispersion in epileptic children. Acta Paediatr. 2003; 92: 916-920.
24. Dumaine R, Antzelevitch C. Molecular mechanisms underlying the long QT syndrome. Curr Opin Cardiol. 2002; 17: 36-42.
25. Racine RJ, Gartner JG, Burnham WM. Epileptiform activity and neural plasticity in limbic structures. Brain Res. 1972; 47: 262-268.
26. Barajas-Martinez H, Haufe V, Chamberland C, Roy MJ, Fecteau MH, Cordeiro JM, Dumaine R. Larger dispersion of INa in female dog ventricle as a mechanism for gender-specific incidence of cardiac arrhythmias. Cardiovasc Res. 2009; 81: 82-89. doi: 10. 1093/cvr/cvn255.
27. Haufe V, Cordeiro JM, Zimmer T, Wu YS, Schiccitano S, Benndorf K, Dumaine R. Contribution of neuronal sodium channels to the cardiac fast sodium current INa is greater in dog heart Purkinje fibers than in ventricles. Cardiovasc Res. 2005; 65: 117-127. doi: 10. 1016/j. cardiores. 2004. 08. 017.
28. Wendt DJ, Starmer CF, Grant AO. Na channel kinetics remain stable during perforated-patch recordings. Am J Physiol. 1992; 263: C1234-C1240.
29. Zimmer T, Biskup C, Dugarmaa S, Vogel F, Steinbis M, Böhle T, Wu YS, Dumaine R, Benndorf K. Functional expression of GFP-linked human heart sodium channel (hH1) and subcellular localization of the a subunit in HEK293 cells and dog cardiac myocytes. J Membr Biol. 2002; 186: 1-12. doi: 10. 1007/s00232-001-0130-1.
30. Ramakers C, Vos MA, Doevendans PA, Schoenmakers M, Wu YS, Scicchitano S, Iodice A, Thomas GP, Antzelevitch C, Dumaine R. Coordinated down-regulation of KCNQ1 and KCNE1 expression contributes to reduction of I(Ks) in canine hypertrophied hearts. Cardiovasc Res. 2003; 57: 486-496.
31. Haufe V, Camacho JA, Dumaine R, Günther B, Bollensdorff C, von Banchet GS, Benndorf K, Zimmer T. Expression pattern of neuronal and skeletal muscle voltage-gated Na+ channels in the developing mouse heart. J Physiol. 2005; 564(Pt 3): 683-696. doi: 10. 1113/jphysiol. 2004. 079681.
32. Gavillet B, Rougier JS, Domenighetti AA, Behar R, Boixel C, Ruchat P, Lehr HA, Pedrazzini T, Abriel H. Cardiac sodium channel Nav1. 5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ Res. 2006; 99: 407-414. doi: 10. 1161/01. RES. 0000237466. 13252. 5e.
33. Li GR, Sun HY, Chen JB, Zhou Y, Tse HF, Lau CP. Characterization of multiple ion channels in cultured human cardiac fibroblasts. PLoS One. 2009; 4: e7307. doi: 10. 1371/journal. pone. 0007307.
34. Auld VJ, Goldin AL, Krafte DS, Marshall J, Dunn JM, Catterall WA, Lester HA, Davidson N, Dunn RJ. A rat brain Na+ channel alpha subunit with novel gating properties. Neuron. 1988; 1: 449-461.
35. Nuss HB, Chiamvimonvat N, Pérez-García MT, Tomaselli GF, Marbán E. Functional association of the beta 1 subunit with human cardiac (hH1) and rat skeletal muscle (mu 1) sodium channel alpha subunits expressed in Xenopus oocytes. J Gen Physiol. 1995; 106: 1171-1191.
36. Chahine M, Deschene I, Chen LQ, Kallen RG. Electrophysiological characteristics of cloned skeletal and cardiac muscle sodium channels. Am J Physiol. 1996; 271(2 Pt 2): H498-H506.
37. Segal MM, Douglas AF. Late sodium channel openings underlying epileptiform activity are preferentially diminished by the anticonvulsant phenytoin. J Neurophysiol. 1997; 77: 3021-3034.
38. Vanoye CG, Lossin C, Rhodes TH, George AL Jr. Single-channel properties of human NaV1. 1 and mechanism of channel dysfunction in SCN1A-associated epilepsy. J Gen Physiol. 2006; 127: 1-14. doi: 10. 1085/ jgp. 200509373.
39. Chen S, Su H, Yue C, Remy S, Royeck M, Sochivko D, Opitz T, Beck H, Yaari Y. An increase in persistent sodium current contributes to intrinsic neuronal bursting after status epilepticus. J Neurophysiol. 2011; 105: 117-129. doi: 10. 1152/jn. 00184. 2010.
40. Xu X, Guo F, Lv X, Feng R, Min D, Ma L, Liu Y, Zhao J, Wang L, Chen T, Shaw C, Hao L, Cai J. Abnormal changes in voltage-gated sodium channels Na(V)1. 1, Na(V)1. 2, Na(V)1. 3, Na(V)1. 6 and in calmodulin/calmodulin-dependent protein kinase II, within the brains of spontaneously epileptic rats and tremor rats. Brain Res Bull. 2013; 96: 1-9. doi: 10. 1016/j. brainresbull. 2013. 04. 003.
41. Biet M, Barajas-Martínez H, Ton AT, Delabre JF, Morin N, Dumaine R. About half of the late sodium current in cardiac myocytes from dog ventricle is due to non-cardiac-type Na(+) channels. J Mol Cell Cardiol. 2012; 53: 593-598. doi: 10. 1016/j. yjmcc. 2012. 06. 012.
42. Haufe V, Chamberland C, Dumaine R. The promiscuous nature of the cardiac sodium current. J Mol Cell Cardiol. 2007; 42: 469-477. doi: 10. 1016/j. yjmcc. 2006. 12. 005.
43. Yoo S, Dobrzynski H, Fedorov VV, Xu SZ, Yamanushi TT, Jones SA, Yamamoto M, Nikolski VP, Efimov IR, Boyett MR. Localization of Na+ channel isoforms at the atrioventricular junction and atrioventricular node in the rat. Circulation. 2006; 114: 1360-1371. doi: 10. 1161/ CIRCULATIONAHA. 106. 613182.
44. Westenbroek RE, Bischoff S, Fu Y, Maier SK, Catterall WA, Scheuer T. Localization of sodium channel subtypes in mouse ventricular myocytes using quantitative immunocytochemistry. J Mol Cell Cardiol. 2013; 64: 69-78. doi: 10. 1016/j. yjmcc. 2013. 08. 004.
45. Aman TK, Grieco-Calub TM, Chen C, Rusconi R, Slat EA, Isom LL, Raman IM. Regulation of persistent Na current by interactions between beta subunits of voltage-gated Na channels. J Neurosci. 2009; 29: 2027-2042. doi: 10. 1523/JNEUROSCI. 4531-08. 2009.
46. Kiss T. Persistent Na-channels: origin and function. A review. Acta Biol Hung. 2008; 59 Suppl: 1-12. doi: 10. 1556/ABiol. 59. 2008. Suppl. 1.
47. Mantegazza M, Yu FH, Powell AJ, Clare JJ, Catterall WA, Scheuer T. Molecular determinants for modulation of persistent sodium current by G-protein betagamma subunits. J Neurosci. 2005; 25: 3341-3349. doi: 10. 1523/JNEUROSCI. 0104-05. 2005.
48. Besana A, Wang DW, George AL Jr, Schwartz PJ. Nadolol block of Nav1. 5 does not explain its efficacy in the long QT syndrome. J Cardiovasc Pharmacol. 2012; 59: 249-253. doi: 10. 1097/FJC. 0b013e31823d2fd1.
49. Antzelevitch C, Burashnikov A, Sicouri S, Belardinelli L. Electrophysiologic basis for the antiarrhythmic actions of ranolazine. Heart Rhythm. 2011; 8: 1281-1290. doi: 10. 1016/j. hrthm. 2011. 03. 045.
50. Drake ME, Reider CR, Kay A. Electrocardiography in epilepsy patients without cardiac symptoms. Seizure. 1993; 2: 63-65.