Increased expression of HCN channels in the ventricular myocardium contributes to enhanced arrhythmicity in mouse failing hearts

Journal of the American Heart Association

Volumn 2, Issue 3, 2013, Pages

  Kuwabara, Yoshihiro ^a   Kuwahara, Koichiro ^a   Takano, Makoto ^b   Kinoshita, Hideyuki ^a   Arai, Yuji ^c   Yasuno, Shinji ^a   Nakagawa, Yasuaki ^a   Igata, Sachiyo ^b   Usami, Satoru ^a   Minami, Takeya ^a   Yamada, Yuko ^a   Nakao, Kazuhiro ^a   Yamada, Chinatsu ^a   Shibata, Junko ^a   Nishikimi, Toshio ^a   Ueshima, Kenji ^a   Nakao, Kazuwa ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c Center Research Institute ^*  (Japan)

Author keywords

Arrhythmia; HCN channel; Heart failure; Ion channels

Indexed keywords

BETA ADRENERGIC RECEPTOR; CYCLIC NUCLEOTIDE GATED CHANNEL; HYPERPOLARIZATION ACTIVATED CATION CHANNEL 2; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; IVABRADINE; UNCLASSIFIED DRUG; BENZAZEPINE DERIVATIVE; CATION; ION CHANNEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; BETA ADRENERGIC STIMULATION; CELL ISOLATION; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; DRUG EFFICACY; EMBRYO; HEART ARRHYTHMIA; HEART AUTOMATICITY; HEART DISEASE; HEART FAILURE; HEART FUNCTION; HEART MUSCLE CELL; HEART PROTECTION; HEART RATE; HEART RATE VARIABILITY; HEART VENTRICLE TACHYCARDIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BLOCKING; SUDDEN DEATH; SURVIVAL RATE; SYSTOLIC BLOOD PRESSURE; TRANSGENIC MOUSE; TREATMENT OUTCOME; VENTRICULAR NONCOMPACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; ARRHYTHMIAS, CARDIAC; BIOSYNTHESIS; COMPLICATION; HEART VENTRICLE; METABOLISM; DRUG ANTAGONISM;

ANIMALS; ARRHYTHMIAS, CARDIAC; BENZAZEPINES; CATIONS; HEART FAILURE; HEART VENTRICLES; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MICE; MICE, TRANSGENIC;

ARRHYTHMIA; HCN CHANNEL; HEART FAILURE; ION CHANNELS;

EID: 84886456842     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.113.000150     Document Type: Article

References (43)

1. Tomaselli GF, Marban E. Electrophysiological remodeling in hypertrophy and heart failure. Cardiovasc Res. 1999;42:270-283.
2. Robinson RB, Siegelbaum SA. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu Rev Physiol. 2003;65:453-480.
3. Wahl-Schott C, Biel M. HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci. 2009;66:470-494.
4. Yasui K, Liu W, Opthof T, Kada K, Lee JK, Kamiya K, Kodama I. I(f) current and spontaneous activity in mouse embryonic ventricular myocytes. Circ Res. 2001;88:536-542.
5. Cerbai E, Pino R, Sartiani L, Mugelli A. Influence of postnatal-development on I (f) occurrence and properties in neonatal rat ventricular myocytes. Cardiovasc Res. 1999;42:416-423.
6. Cerbai E, Mugelli A. I(f) in non-pacemaker cells: role and pharmacological implications. Pharmacol Res. 2006;53:416-423.
7. Stillitano F, Lonardo G, Zicha S, Varro A, Cerbai E, Mugelli A, Nattel S. Molecular basis of funny current (If) in normal and failing human heart. J Mol Cell Cardiol. 2008;45:289-299.
8. Kuwahara K, Saito Y, Ogawa E, Takahashi N, Nakagawa Y, Naruse Y, Harada M, Hamanaka I, Izumi T, Miyamoto Y, Kishimoto I, Kawakami R, Nakanishi M, Mori N, Nakao K. The neuron-restrictive silencer element-neuron-restrictive silencer factor system regulates basal and endothelin 1-inducible atrial natriuretic peptide gene expression in ventricular myocytes. Mol Cell Biol. 2001; 21:2085-2097.
9. Kuwahara K, Saito Y, Takano M, Arai Y, Yasuno S, Nakagawa Y, Takahashi N, Adachi Y, Takemura G, Horie M, Miyamoto Y, Morisaki T, Kuratomi S, Noma A, Fujiwara H, Yoshimasa Y, Kinoshita H, Kawakami R, Kishimoto I, Nakanishi M, Usami S, Saito Y, Harada M, Nakao K. NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J. 2003; 22:6310-6321.
10. Xia S, Wang Y, Zhang Y, Deng SB, Du JL, Wang XC, She Q. Dynamic changes in HCN2, HCN4, KCNE1, and KCNE2 expression in ventricular cells from acute myocardial infarction rat hearts. Biochem Biophys Res Commun. 2010; 395:330-335.
11. Fernandez-Velasco M, Ruiz-Hurtado G, Delgado C. I K1 and I f in ventricular myocytes isolated from control and hypertrophied rat hearts. Pflugers Arch. 2006;452:146-154.
12. Du XJ, Feng X, Gao XM, Tan TP, Kiriazis H, Dart AM. I(f) channel inhibitor ivabradine lowers heart rate in mice with enhanced sympathoadrenergic activities. Br J Pharmacol. 2004;142:107-112.
13. Leoni AL, Marionneau C, Demolombe S, Le Bouter S, Mangoni ME, Escande D, Charpentier F. Chronic heart rate reduction remodels ion channel transcripts in the mouse sinoatrial node but not in the ventricle. Physiol Genomics. 2005;24:4-12.
14. Kinoshita H, Kuwahara K, Takano M, Arai Y, Kuwabara Y, Yasuno S, Nakagawa Y, Nakanishi M, Harada M, Fujiwara M, Murakami M, Ueshima K, Nakao K. T-type Ca2+ channel blockade prevents sudden death in mice with heart failure. Circulation. 2009;120:743-752.
15. Bucchi A, Tognati A, Milanesi R, Baruscotti M, DiFrancesco D. Properties of ivabradine-induced block of HCN1 and HCN4 pacemaker channels. J Physiol. 2006;572:335-346.
16. Gehrmann J, Berul CI. Cardiac electrophysiology in genetically engineered mice. J Cardiovasc Electrophysiol. 2000;11:354-368.
17. Kawakami R, Saito Y, Kishimoto I, Harada M, Kuwahara K, Takahashi N, Nakagawa Y, Nakanishi M, Tanimoto K, Usami S, Yasuno S, Kinoshita H, Chusho H, Tamura N, Ogawa Y, Nakao K. Overexpression of brain natriuretic peptide facilitates neutrophil infiltration and cardiac matrix metalloproteinase-9 expression after acute myocardial infarction. Circulation. 2004;110:3306-3312.
18. Just A, Faulhaber J, Ehmke H. Autonomic cardiovascular control in conscious mice. Am J Physiol Regul Integr Comp Physiol. 2000;279:R2214-R2221.
19. Stieber J, Wieland K, Stockl G, Ludwig A, Hofmann F. Bradycardic and proarrhythmic properties of sinus node inhibitors. Mol Pharmacol. 2006;69: 1328-1337.
20. Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, Shirakami G, Jougasaki M, Obata K, Yasue H, Kambayashi Y, Inouye K, Imura H. Brain natriuretic peptide as a novel cardiac hormone in humans. Evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J Clin Invest. 1991;87:1402-1412.
21. Nakagawa O, Ogawa Y, Itoh H, Suga S, Komatsu Y, Kishimoto I, Nishino K, Yoshimasa T, Nakao K. Rapid transcriptional activation and early mrna turnover of brain natriuretic peptide in cardiocyte hypertrophy. Evidence for brain natriuretic peptide as an "emergency" cardiac hormone against ventricular overload. J Clin Invest. 1995;96:1280-1287.
22. La Rovere MT, Pinna GD, Maestri R, Mortara A, Capomolla S, Febo O, Ferrari R, Franchini M, Gnemmi M, Opasich C, Riccardi PG, Traversi E, Cobelli F. Shortterm heart rate variability strongly predicts sudden cardiac death in chronic heart failure patients. Circulation. 2003;107:565-570.
23. Sandercock GR, Brodie DA. The role of heart rate variability in prognosis for different modes of death in chronic heart failure. Pacing Clin Electrophysiol. 2006;29:892-904.
24. Takano M, Kinoshita H, Shioya T, Itoh M, Nakao K, Kuwahara K. Pathophysiological remodeling of mouse cardiac myocytes expressing dominant negative mutant of neuron restrictive silencing factor. Circ J. 2010;74:2712- 2719.
25. Kuratomi S, Ohmori Y, Ito M, Shimazaki K, Muramatsu S, Mizukami H, Uosaki H, Yamashita JK, Arai Y, Kuwahara K, Takano M. The cardiac pacemakerspecific channel HCN4 is a direct transcriptional target of MEF2. Cardiovasc Res. 2009;83:682-687.
26. Kuratomi S, Kuratomi A, Kuwahara K, Ishii TM, Nakao K, Saito Y, Takano M. NRSF regulates the developmental and hypertrophic changes of HCN4 transcription in rat cardiac myocytes. Biochem Biophys Res Commun. 2007; 353:67-73.
27. Baruscotti M, Bucchi A, Viscomi C, Mandelli G, Consalez G, Gnecchi-Rusconi T, Montano N, Casali KR, Micheloni S, Barbuti A, DiFrancesco D. Deep bradycardia and heart block caused by inducible cardiac-specific knockout of the pacemaker channel gene HCN4. Proc Natl Acad Sci USA. 2011; 108:1705-1710.
28. Riccioni G. Ivabradine: recent and potential applications in clinical practice. Expert Opin Pharmacother. 2011;12:443-450.
29. Bohm M, Swedberg K, Komajda M, Borer JS, Ford I, Dubost-Brama A, Lerebours G, Tavazzi L. Heart rate as a risk factor in chronic heart failure (SHIFT): the association between heart rate and outcomes in a randomised placebo-controlled trial. Lancet. 2010;376:886-894.
30. Fox K, Borer JS, Camm AJ, Danchin N, Ferrari R, Lopez Sendon JL, Steg PG, Tardif JC, Tavazzi L, Tendera M. Resting heart rate in cardiovascular disease. J Am Coll Cardiol. 2007;50:823-830.
31. Swedberg K, Komajda M, Bohm M, Borer JS, Ford I, Dubost-Brama A, Lerebours G, Tavazzi L. Ivabradine and outcomes in chronic heart failure (SHIFT): a randomised placebo-controlled study. Lancet. 2010;376: 875-885.
32. Heusch G, Skyschally A, Schulz R. Cardioprotection by ivabradine through heart rate reduction and beyond. J Cardiovasc Pharmacol Ther. 2011;16:281- 284.
33. Ceconi C, Freedman SB, Tardif JC, Hildebrandt P, McDonagh T, Gueret P, Parrinello G, Robertson M, Steg PG, Tendera M, Ford I, Fox K, Ferrari R. Effect of heart rate reduction by ivabradine on left ventricular remodeling in the echocardiographic substudy of beautiful. Int J Cardiol. 2011;146:408- 414.
34. Fox K, Ford I, Steg PG, Tendera M, Ferrari R. Ivabradine for patients with stable coronary artery disease and left-ventricular systolic dysfunction (BEAUTIFUL): a randomised, double-blind, placebo-controlled trial. Lancet. 2008;372:807- 816.
35. Tardif JC, O'Meara E, Komajda M, Bohm M, Borer JS, Ford I, Tavazzi L, Swedberg K. Effects of selective heart rate reduction with ivabradine on left ventricular remodelling and function: results from the shift echocardiography substudy. Eur Heart J. 2011;32:2507-2515.
36. Boukens BJ, Christoffels VM, Coronel R, Moorman AF. Developmental basis for electrophysiological heterogeneity in the ventricular and outflow tract myocardium as a substrate for life-threatening ventricular arrhythmias. Circ Res. 2009;104:19-31.
37. Sasyniuk BI. Symposium on the management of ventricular dysrhythmias. Concept of reentry versus automaticity. Am J Cardiol. 1984;54:1A-6A.
38. Hofmann F, Fabritz L, Stieber J, Schmitt J, Kirchhof P, Ludwig A, Herrmann S. Ventricular HCN channels decrease the repolarization reserve in the hypertrophic heart. Cardiovasc Res. 2012;95:317-326.
39. Fenske S, Krause S, Biel M, Wahl-Schott C. The role of HCN channels in ventricular repolarization. Trends Cardiovasc Med. 2011;21:216-220.
40. DiFrancesco D. The role of the funny current in pacemaker activity. Circ Res. 2010;106:434-446.
41. Effect of metoprolol CR/XL in chronic heart failure: metoprolol CR/XL randomised intervention trial in congestive heart failure (MERIT-HF). Lancet. 1999;353:2001-2007.
42. Packer M, Fowler MB, Roecker EB, Coats AJ, Katus HA, Krum H, Mohacsi P, Rouleau JL, Tendera M, Staiger C, Holcslaw TL, Amann-Zalan I, DeMets DL. Effect of carvedilol on the morbidity of patients with severe chronic heart failure: results of the carvedilol prospective randomized cumulative survival (COPERNICUS) study. Circulation. 2002;106:2194-2199.
43. Swedberg K, Komajda M, Bohm M, Borer J, Robertson M, Tavazzi L, Ford I. Effects on outcomes of heart rate reduction by ivabradine in patients with congestive heart failure: is there an influence of beta-blocker dose? Findings from the SHIFT (systolic heart failure treatment with the I(f) inhibitor ivabradine trial) study. J Am Coll Cardiol. 2012;59: 1938-1945.