Skip to main content
Erschienen in: Heart and Vessels 7/2018

18.01.2018 | Original Article

A mutant HCN4 channel in a family with bradycardia, left bundle branch block, and left ventricular noncompaction

verfasst von: Ryosuke Yokoyama, Koshi Kinoshita, Yukiko Hata, Masayoshi Abe, Kenta Matsuoka, Keiichi Hirono, Masanobu Kano, Makoto Nakazawa, Fukiko Ichida, Naoki Nishida, Toshihide Tabata

Erschienen in: Heart and Vessels | Ausgabe 7/2018

Einloggen, um Zugang zu erhalten

Abstract

We found that a female infant presenting with left bundle branch block and left ventricular noncompaction carries uninvestigated gene mutations HCN4(G811E), SCN5A(L1988R), DMD(S2384Y), and EMD(R203H). Here, we explored the possible pathogenicity of HCN4(G811E), which results in a G811E substitution in hyperpolarization-activated cyclic nucleotide-gated channel 4, the main subunit of the cardiac pacemaker channel. Voltage-clamp measurements in a heterologous expression system of HEK293T cells showed that HCN4(G811E) slightly reduced whole-cell HCN4 channel conductance, whereas it did not affect the gating kinetics, unitary conductance, or cAMP-dependent modulation of voltage-dependence. Immunocytochemistry and immunoblot analysis showed that the G811E mutation did not impair the membrane trafficking of the channel subunit in the heterologous expression system. These findings indicate that HCN4(G811E) may not be a monogenic factor to cause the cardiac disorders.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Shi W, Wymore R, Yu H, Wu J, Wymore RT, Pan Z, Robinson RB, Dixon JE, McKinnon D, Cohen IS (1999) Distribution and prevalence of hyperpolarization-activated cation channel (HCN) mRNA expression in cardiac tissues. Circ Res 85:e1–e6CrossRefPubMed Shi W, Wymore R, Yu H, Wu J, Wymore RT, Pan Z, Robinson RB, Dixon JE, McKinnon D, Cohen IS (1999) Distribution and prevalence of hyperpolarization-activated cation channel (HCN) mRNA expression in cardiac tissues. Circ Res 85:e1–e6CrossRefPubMed
2.
Zurück zum Zitat Verkerk AO, Wilders R (2014) Pacemaker activity of the human sinoatrial node: effects of HCN4 mutations on the hyperpolarization-activated current. Europace 16:384–395CrossRefPubMed Verkerk AO, Wilders R (2014) Pacemaker activity of the human sinoatrial node: effects of HCN4 mutations on the hyperpolarization-activated current. Europace 16:384–395CrossRefPubMed
4.
Zurück zum Zitat Duhme N, Schweizer PA, Thomas D, Becker R, Schroter J, Barends TR, Schlichting I, Draguhn A, Bruehl C, Katus HA, Koenen M (2013) Altered HCN4 channel C-linker interaction is associated with familial tachycardia-bradycardia syndrome and atrial fibrillation. Eur Heart J 34:2768–2775CrossRefPubMed Duhme N, Schweizer PA, Thomas D, Becker R, Schroter J, Barends TR, Schlichting I, Draguhn A, Bruehl C, Katus HA, Koenen M (2013) Altered HCN4 channel C-linker interaction is associated with familial tachycardia-bradycardia syndrome and atrial fibrillation. Eur Heart J 34:2768–2775CrossRefPubMed
5.
Zurück zum Zitat Schweizer PA, Duhme N, Thomas D, Becker R, Zehelein J, Draguhn A, Bruehl C, Katus HA, Koenen M (2010) cAMP sensitivity of HCN pacemaker channels determines basal heart rate but is not critical for autonomic rate control. Circ Arrhythm Electrophysiol 3:542–552CrossRefPubMed Schweizer PA, Duhme N, Thomas D, Becker R, Zehelein J, Draguhn A, Bruehl C, Katus HA, Koenen M (2010) cAMP sensitivity of HCN pacemaker channels determines basal heart rate but is not critical for autonomic rate control. Circ Arrhythm Electrophysiol 3:542–552CrossRefPubMed
6.
Zurück zum Zitat Schulze-Bahr E, Neu A, Friederich P, Kaupp UB, Breithardt G, Pongs O, Isbrandt D (2003) Pacemaker channel dysfunction in a patient with sinus node disease. J Clin Investig 111:1537–1545CrossRefPubMedPubMedCentral Schulze-Bahr E, Neu A, Friederich P, Kaupp UB, Breithardt G, Pongs O, Isbrandt D (2003) Pacemaker channel dysfunction in a patient with sinus node disease. J Clin Investig 111:1537–1545CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Hategan L, Csanyi B, Ordog B, Kakonyi K, Tringer A, Kiss O, Orosz A, Saghy L, Nagy I, Hegedus Z, Rudas L, Szell M, Varro A, Forster T, Sepp R (2017) A novel ‘splice site’ HCN4 Gene mutation, c.1737 + 1 G>T, causes familial bradycardia, reduced heart rate response, impaired chronotropic competence and increased short-term heart rate variability. Int J Cardiol 241:364–372CrossRefPubMed Hategan L, Csanyi B, Ordog B, Kakonyi K, Tringer A, Kiss O, Orosz A, Saghy L, Nagy I, Hegedus Z, Rudas L, Szell M, Varro A, Forster T, Sepp R (2017) A novel ‘splice site’ HCN4 Gene mutation, c.1737 + 1 G>T, causes familial bradycardia, reduced heart rate response, impaired chronotropic competence and increased short-term heart rate variability. Int J Cardiol 241:364–372CrossRefPubMed
8.
Zurück zum Zitat Milano A, Vermeer AM, Lodder EM, Barc J, Verkerk AO, Postma AV, van der Bilt IA, Baars MJ, van Haelst PL, Caliskan K, Hoedemaekers YM, Le Scouarnec S, Redon R, Pinto YM, Christiaans I, Wilde AA, Bezzina CR (2014) HCN4 mutations in multiple families with bradycardia and left ventricular noncompaction cardiomyopathy. J Am Coll Cardiol 64:745–756CrossRefPubMed Milano A, Vermeer AM, Lodder EM, Barc J, Verkerk AO, Postma AV, van der Bilt IA, Baars MJ, van Haelst PL, Caliskan K, Hoedemaekers YM, Le Scouarnec S, Redon R, Pinto YM, Christiaans I, Wilde AA, Bezzina CR (2014) HCN4 mutations in multiple families with bradycardia and left ventricular noncompaction cardiomyopathy. J Am Coll Cardiol 64:745–756CrossRefPubMed
9.
Zurück zum Zitat Schweizer PA, Schröter J, Greiner S, Haas J, Yampolsky P, Mereles D, Buss SJ, Seyler C, Bruehl C, Draguhn A, Koenen M, Meder B, Katus HA, Thomas D (2014) The symptom complex of familial sinus node dysfunction and myocardial noncompaction is associated with mutations in the HCN4 channel. J Am Coll Cardiol 64:757–767CrossRefPubMed Schweizer PA, Schröter J, Greiner S, Haas J, Yampolsky P, Mereles D, Buss SJ, Seyler C, Bruehl C, Draguhn A, Koenen M, Meder B, Katus HA, Thomas D (2014) The symptom complex of familial sinus node dysfunction and myocardial noncompaction is associated with mutations in the HCN4 channel. J Am Coll Cardiol 64:757–767CrossRefPubMed
10.
Zurück zum Zitat Liang X, Evans SM, Sun Y (2015) Insights into cardiac conduction system formation provided by HCN4 expression. Trends Cardiovasc Med 25:1–9CrossRefPubMed Liang X, Evans SM, Sun Y (2015) Insights into cardiac conduction system formation provided by HCN4 expression. Trends Cardiovasc Med 25:1–9CrossRefPubMed
11.
Zurück zum Zitat Ichida F, Tsubata S, Bowles KR, Haneda N, Uese K, Miyawaki T, Dreyer WJ, Messina J, Li H, Bowles NE, Towbin JA (2001) Novel gene mutations in patients with left ventricular noncompaction or Barth syndrome. Circulation 103:1256–1263CrossRefPubMed Ichida F, Tsubata S, Bowles KR, Haneda N, Uese K, Miyawaki T, Dreyer WJ, Messina J, Li H, Bowles NE, Towbin JA (2001) Novel gene mutations in patients with left ventricular noncompaction or Barth syndrome. Circulation 103:1256–1263CrossRefPubMed
12.
Zurück zum Zitat Hata Y, Kinoshita K, Mizumaki K, Yamaguchi Y, Hirono K, Ichida F, Takasaki A, Mori H, Nishida N (2016) Postmortem genetic analysis of sudden unexplained death syndrome under 50 years of age: a next-generation sequencing study. Heart Rhythm 13:1544–1551CrossRefPubMed Hata Y, Kinoshita K, Mizumaki K, Yamaguchi Y, Hirono K, Ichida F, Takasaki A, Mori H, Nishida N (2016) Postmortem genetic analysis of sudden unexplained death syndrome under 50 years of age: a next-generation sequencing study. Heart Rhythm 13:1544–1551CrossRefPubMed
13.
Zurück zum Zitat Yamaguchi Y, Nishide K, Kato M, Hata Y, Mizumaki K, Kinoshita K, Nonobe Y, Tabata T, Sakamoto T, Kataoka N, Nakatani Y, Ichida F, Mori H, Fukurotani K, Inoue H, Nishida N (2014) Glycine/serine polymorphism at position 38 influences KCNE1 subunit’s modulatory actions on rapid and slow delayed rectifier K+ currents. Circ J 78:610–618CrossRefPubMed Yamaguchi Y, Nishide K, Kato M, Hata Y, Mizumaki K, Kinoshita K, Nonobe Y, Tabata T, Sakamoto T, Kataoka N, Nakatani Y, Ichida F, Mori H, Fukurotani K, Inoue H, Nishida N (2014) Glycine/serine polymorphism at position 38 influences KCNE1 subunit’s modulatory actions on rapid and slow delayed rectifier K+ currents. Circ J 78:610–618CrossRefPubMed
14.
Zurück zum Zitat Maekawa K, Saito Y, Ozawa S, Adachi-Akahane S, Kawamoto M, Komamura K, Shimizu W, Ueno K, Kamakura S, Kamatani N, Kitakaze M, Sawada J (2005) Genetic polymorphisms and haplotypes of the human cardiac sodium channel alpha subunit gene (SCN5A) in Japanese and their association with arrhythmia. Ann Hum Genet 69:413–428CrossRefPubMed Maekawa K, Saito Y, Ozawa S, Adachi-Akahane S, Kawamoto M, Komamura K, Shimizu W, Ueno K, Kamakura S, Kamatani N, Kitakaze M, Sawada J (2005) Genetic polymorphisms and haplotypes of the human cardiac sodium channel alpha subunit gene (SCN5A) in Japanese and their association with arrhythmia. Ann Hum Genet 69:413–428CrossRefPubMed
15.
Zurück zum Zitat Lee YS, Olaopa MA, Jung BC, Lee SH, Shin DG, Park HS, Cho Y, Han SM, Lee MH, Kim YN (2016) Genetic variation of SCN5A in Korean patients with sick sinus syndrome. Korean Circ J 46:63–71CrossRefPubMedPubMedCentral Lee YS, Olaopa MA, Jung BC, Lee SH, Shin DG, Park HS, Cho Y, Han SM, Lee MH, Kim YN (2016) Genetic variation of SCN5A in Korean patients with sick sinus syndrome. Korean Circ J 46:63–71CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Hussein A, Karimianpour A, Collier P, Krasuski RA (2015) Isolated noncompaction of the left ventricle in adults. J Am Coll Cardiol 66:578–585CrossRefPubMed Hussein A, Karimianpour A, Collier P, Krasuski RA (2015) Isolated noncompaction of the left ventricle in adults. J Am Coll Cardiol 66:578–585CrossRefPubMed
17.
Zurück zum Zitat Ohno S, Omura M, Kawamura M, Kimura H, Itoh H, Makiyama T, Ushinohama H, Makita N, Horie M (2014) Exon 3 deletion of RYR2 encoding cardiac ryanodine receptor is associated with left ventricular non-compaction. Europace 16:1646–1654CrossRefPubMed Ohno S, Omura M, Kawamura M, Kimura H, Itoh H, Makiyama T, Ushinohama H, Makita N, Horie M (2014) Exon 3 deletion of RYR2 encoding cardiac ryanodine receptor is associated with left ventricular non-compaction. Europace 16:1646–1654CrossRefPubMed
18.
Zurück zum Zitat Towbin JA, Lorts A, Jefferies JL (2015) Left ventricular non-compaction cardiomyopathy. Lancet 386(9995):813–825CrossRefPubMed Towbin JA, Lorts A, Jefferies JL (2015) Left ventricular non-compaction cardiomyopathy. Lancet 386(9995):813–825CrossRefPubMed
19.
Zurück zum Zitat Lolicato M, Bucchi A, Arrigoni C, Zucca S, Nardini M, Schroeder I, Simmons K, Aquila M, DiFrancesco D, Bolognesi M, Schwede F, Kashin D, Fishwick CW, Johnson AP, Thiel G, Moroni A (2014) Cyclic dinucleotides bind the C-linker of HCN4 to control channel cAMP responsiveness. Nat Chem Biol 10:457–462CrossRefPubMed Lolicato M, Bucchi A, Arrigoni C, Zucca S, Nardini M, Schroeder I, Simmons K, Aquila M, DiFrancesco D, Bolognesi M, Schwede F, Kashin D, Fishwick CW, Johnson AP, Thiel G, Moroni A (2014) Cyclic dinucleotides bind the C-linker of HCN4 to control channel cAMP responsiveness. Nat Chem Biol 10:457–462CrossRefPubMed
20.
Zurück zum Zitat DiFrancesco D (2010) The role of the funny current in pacemaker activity. Circ Res 106:434–446CrossRefPubMed DiFrancesco D (2010) The role of the funny current in pacemaker activity. Circ Res 106:434–446CrossRefPubMed
21.
Zurück zum Zitat Liao Z, Lockhead D, St Clair JR, Larson ED, Wilson CE, Proenza C (2012) Cellular context and multiple channel domains determine cAMP sensitivity of HCN4 channels: ligand-independent relief of autoinhibition in HCN4. J Gen Physiol 140:557–566CrossRefPubMedPubMedCentral Liao Z, Lockhead D, St Clair JR, Larson ED, Wilson CE, Proenza C (2012) Cellular context and multiple channel domains determine cAMP sensitivity of HCN4 channels: ligand-independent relief of autoinhibition in HCN4. J Gen Physiol 140:557–566CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat DiFrancesco D, Tortora P (1991) Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351:145–147CrossRefPubMed DiFrancesco D, Tortora P (1991) Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351:145–147CrossRefPubMed
23.
24.
Zurück zum Zitat Laish-Farkash A, Glikson M, Brass D, Marek-Yagel D, Pras E, Dascal N, Antzelevitch C, Nof E, Reznik H, Eldar M, Luria D (2010) A novel mutation in the HCN4 gene causes symptomatic sinus bradycardia in Moroccan Jews. J Cardiovasc Electrophysiol 21:1365–1372CrossRefPubMedPubMedCentral Laish-Farkash A, Glikson M, Brass D, Marek-Yagel D, Pras E, Dascal N, Antzelevitch C, Nof E, Reznik H, Eldar M, Luria D (2010) A novel mutation in the HCN4 gene causes symptomatic sinus bradycardia in Moroccan Jews. J Cardiovasc Electrophysiol 21:1365–1372CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Macri V, Mahida SN, Zhang ML, Sinner MF, Dolmatova EV, Tucker NR, McLellan M, Shea MA, Milan DJ, Lunetta KL, Benjamin EJ, Ellinor PT (2014) A novel trafficking-defective HCN4 mutation is associated with early-onset atrial fibrillation. Heart Rhythm 11:1055–1062CrossRefPubMedPubMedCentral Macri V, Mahida SN, Zhang ML, Sinner MF, Dolmatova EV, Tucker NR, McLellan M, Shea MA, Milan DJ, Lunetta KL, Benjamin EJ, Ellinor PT (2014) A novel trafficking-defective HCN4 mutation is associated with early-onset atrial fibrillation. Heart Rhythm 11:1055–1062CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Nof E, Luria D, Brass D, Marek D, Lahat H, Reznik-Wolf H, Pras E, Dascal N, Eldar M, Glikson M (2007) Point mutation in the HCN4 cardiac ion channel pore affecting synthesis, trafficking, and functional expression is associated with familial asymptomatic sinus bradycardia. Circulation 116:463–470CrossRefPubMed Nof E, Luria D, Brass D, Marek D, Lahat H, Reznik-Wolf H, Pras E, Dascal N, Eldar M, Glikson M (2007) Point mutation in the HCN4 cardiac ion channel pore affecting synthesis, trafficking, and functional expression is associated with familial asymptomatic sinus bradycardia. Circulation 116:463–470CrossRefPubMed
27.
Zurück zum Zitat Baruscotti M, Barbuti A, Bucchi A (2010) The cardiac pacemaker current. J Mol Cell Cardiol 48:55–64CrossRefPubMed Baruscotti M, Barbuti A, Bucchi A (2010) The cardiac pacemaker current. J Mol Cell Cardiol 48:55–64CrossRefPubMed
28.
Zurück zum Zitat Ferlini A, Neri M, Gualandi F (2013) The medical genetics of dystrophinopathies: molecular genetic diagnosis and its impact on clinical practice. Neuromuscul Disord 23:4–14CrossRefPubMed Ferlini A, Neri M, Gualandi F (2013) The medical genetics of dystrophinopathies: molecular genetic diagnosis and its impact on clinical practice. Neuromuscul Disord 23:4–14CrossRefPubMed
29.
Zurück zum Zitat Arbustini E, Weidemann F, Hall JL (2014) Left ventricular noncompaction: a distinct cardiomyopathy or a trait shared by different cardiac diseases? J Am Coll Cardiol 64:1840–1850CrossRefPubMed Arbustini E, Weidemann F, Hall JL (2014) Left ventricular noncompaction: a distinct cardiomyopathy or a trait shared by different cardiac diseases? J Am Coll Cardiol 64:1840–1850CrossRefPubMed
30.
Zurück zum Zitat Kimura K, Morita H, Daimon M, Kawata T, Nakao T, Lee SL, Hirokawa M, Ebihara A, Nakajima T, Ozawa T, Yonemochi Y, Aida I, Motoyoshi Y, Mikata T, Uchida I, Komori T, Kitao R, Nagata T, Takeda S, Komaki H, Segawa K, Takenaka K, Komuro I (2015) Prognostic impact of venous thromboembolism in patients with Duchenne muscular dystrophy: prospective multicenter 5-year cohort study. Int J Cardiol 191:178–180CrossRefPubMed Kimura K, Morita H, Daimon M, Kawata T, Nakao T, Lee SL, Hirokawa M, Ebihara A, Nakajima T, Ozawa T, Yonemochi Y, Aida I, Motoyoshi Y, Mikata T, Uchida I, Komori T, Kitao R, Nagata T, Takeda S, Komaki H, Segawa K, Takenaka K, Komuro I (2015) Prognostic impact of venous thromboembolism in patients with Duchenne muscular dystrophy: prospective multicenter 5-year cohort study. Int J Cardiol 191:178–180CrossRefPubMed
31.
Zurück zum Zitat Parent JJ, Moore RA, Taylor MD, Towbin JA, Jefferies JL (2015) Left ventricular noncompaction cardiomyopathy in Duchenne muscular dystrophy carriers. J Cardiol Cases 11:7–9CrossRef Parent JJ, Moore RA, Taylor MD, Towbin JA, Jefferies JL (2015) Left ventricular noncompaction cardiomyopathy in Duchenne muscular dystrophy carriers. J Cardiol Cases 11:7–9CrossRef
32.
Zurück zum Zitat Meinke P, Nguyen TD, Wehnert MS (2011) The LINC complex and human disease. Biochem Soc Trans 39:1693–1697CrossRefPubMed Meinke P, Nguyen TD, Wehnert MS (2011) The LINC complex and human disease. Biochem Soc Trans 39:1693–1697CrossRefPubMed
33.
Zurück zum Zitat Yuan J, Xue B (2015) Role of structural flexibility in the evolution of emerin. J Theor Biol 385:102–111CrossRefPubMed Yuan J, Xue B (2015) Role of structural flexibility in the evolution of emerin. J Theor Biol 385:102–111CrossRefPubMed
34.
Zurück zum Zitat Parmar MS, Parmar KS (2012) Emery-Dreifuss humeroperoneal muscular dystrophy: cardiac manifestations. Can J Cardiol 28(4):516.e1–516.e3CrossRef Parmar MS, Parmar KS (2012) Emery-Dreifuss humeroperoneal muscular dystrophy: cardiac manifestations. Can J Cardiol 28(4):516.e1–516.e3CrossRef
35.
Zurück zum Zitat Monserrat L, Hermida-Prieto M, Fernandez X, Rodríguez I, Dumont C, Cazón L, Cuesta MG, Gonzalez-Juanatey C, Peteiro J, Álvarez N, Penas-Lado M, Castro-Beiras A (2007) Mutation in the alpha-cardiac actin gene associated with apical hypertrophic cardiomyopathy, left ventricular non-compaction, and septal defects. Eur Heart J 28:1953–1961CrossRefPubMed Monserrat L, Hermida-Prieto M, Fernandez X, Rodríguez I, Dumont C, Cazón L, Cuesta MG, Gonzalez-Juanatey C, Peteiro J, Álvarez N, Penas-Lado M, Castro-Beiras A (2007) Mutation in the alpha-cardiac actin gene associated with apical hypertrophic cardiomyopathy, left ventricular non-compaction, and septal defects. Eur Heart J 28:1953–1961CrossRefPubMed
36.
Zurück zum Zitat Girolami F, Iascone M, Tomberli B, Bardi S, Benelli M, Marseglia G, Pescucci C, Pezzoli L, Sana ME, Basso C, Marziliano N, Merlini PA, Fornaro A, Cecchi F, Torricelli F, Olivotto I (2014) Novel alpha-actinin 2 variant associated with familial hypertrophic cardiomyopathy and juvenile atrial arrhythmias: a massively parallel sequencing study. Circ Cardiovasc Genet 7:741–750CrossRefPubMed Girolami F, Iascone M, Tomberli B, Bardi S, Benelli M, Marseglia G, Pescucci C, Pezzoli L, Sana ME, Basso C, Marziliano N, Merlini PA, Fornaro A, Cecchi F, Torricelli F, Olivotto I (2014) Novel alpha-actinin 2 variant associated with familial hypertrophic cardiomyopathy and juvenile atrial arrhythmias: a massively parallel sequencing study. Circ Cardiovasc Genet 7:741–750CrossRefPubMed
37.
Zurück zum Zitat Stöllberger C, Finsterer J, Blazek G, Bittner RE (1996) Left ventricular non-compaction in a patient with Becker’s muscular dystrophy. Heart 76:380CrossRefPubMedPubMedCentral Stöllberger C, Finsterer J, Blazek G, Bittner RE (1996) Left ventricular non-compaction in a patient with Becker’s muscular dystrophy. Heart 76:380CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Williams T, Machann W, Kuhler L, Hamm H, Muller-Hocker J, Zimmer M, Ertl G, Ritter O, Beer M, Schonberger J (2011) Novel desmoplakin mutation: juvenile biventricular cardiomyopathy with left ventricular non-compaction and acantholytic palmoplantar keratoderma. Clin Res Cardiol 100:1087–1093CrossRefPubMedPubMedCentral Williams T, Machann W, Kuhler L, Hamm H, Muller-Hocker J, Zimmer M, Ertl G, Ritter O, Beer M, Schonberger J (2011) Novel desmoplakin mutation: juvenile biventricular cardiomyopathy with left ventricular non-compaction and acantholytic palmoplantar keratoderma. Clin Res Cardiol 100:1087–1093CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Blinder JJ, Martinez HR, Craigen WJ, Belmont J, Pignatelli RH, Jefferies JL (2011) Noncompaction of the left ventricular myocardium in a boy with a novel chromosome 8p23.1 deletion. Am J Med Genet A 155A:2215–2220CrossRefPubMed Blinder JJ, Martinez HR, Craigen WJ, Belmont J, Pignatelli RH, Jefferies JL (2011) Noncompaction of the left ventricular myocardium in a boy with a novel chromosome 8p23.1 deletion. Am J Med Genet A 155A:2215–2220CrossRefPubMed
40.
Zurück zum Zitat Vatta M, Mohapatra B, Jimenez S, Sanchez X, Faulkner G, Perles Z, Sinagra G, Lin JH, Vu TM, Zhou Q, Bowles KR, Di Lenarda A, Schimmenti L, Fox M, Chrisco MA, Murphy RT, McKenna W, Elliott P, Bowles NE, Chen J, Valle G, Towbin JA (2003) Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 42:2014–2027CrossRefPubMed Vatta M, Mohapatra B, Jimenez S, Sanchez X, Faulkner G, Perles Z, Sinagra G, Lin JH, Vu TM, Zhou Q, Bowles KR, Di Lenarda A, Schimmenti L, Fox M, Chrisco MA, Murphy RT, McKenna W, Elliott P, Bowles NE, Chen J, Valle G, Towbin JA (2003) Mutations in Cypher/ZASP in patients with dilated cardiomyopathy and left ventricular non-compaction. J Am Coll Cardiol 42:2014–2027CrossRefPubMed
41.
Zurück zum Zitat Liu Z, Shan H, Huang J, Li N, Hou C, Pu J (2016) A novel lamin A/C gene missense mutation (445 V > E) in immunoglobulin-like fold associated with left ventricular non-compaction. Europace 18:617–822CrossRefPubMed Liu Z, Shan H, Huang J, Li N, Hou C, Pu J (2016) A novel lamin A/C gene missense mutation (445 V > E) in immunoglobulin-like fold associated with left ventricular non-compaction. Europace 18:617–822CrossRefPubMed
42.
Zurück zum Zitat Wessels MW, Herkert JC, Frohn-Mulder IM, Dalinghaus M, van den Wijngaard A, de Krijger RR, Michels M, de Coo IF, Hoedemaekers YM, Dooijes D (2015) Compound heterozygous or homozygous truncating MYBPC3 mutations cause lethal cardiomyopathy with features of noncompaction and septal defects. Eur J Hum Genet 23:922–928CrossRefPubMed Wessels MW, Herkert JC, Frohn-Mulder IM, Dalinghaus M, van den Wijngaard A, de Krijger RR, Michels M, de Coo IF, Hoedemaekers YM, Dooijes D (2015) Compound heterozygous or homozygous truncating MYBPC3 mutations cause lethal cardiomyopathy with features of noncompaction and septal defects. Eur J Hum Genet 23:922–928CrossRefPubMed
43.
Zurück zum Zitat Hoedemaekers YM, Caliskan K, Majoor-Krakauer D, van de Laar I, Michels M, Witsenburg M, ten Cate FJ, Simoons ML, Dooijes D (2007) Cardiac beta-myosin heavy chain defects in two families with non-compaction cardiomyopathy: linking non-compaction to hypertrophic, restrictive, and dilated cardiomyopathies. Eur Heart J 28:2732–2737CrossRefPubMed Hoedemaekers YM, Caliskan K, Majoor-Krakauer D, van de Laar I, Michels M, Witsenburg M, ten Cate FJ, Simoons ML, Dooijes D (2007) Cardiac beta-myosin heavy chain defects in two families with non-compaction cardiomyopathy: linking non-compaction to hypertrophic, restrictive, and dilated cardiomyopathies. Eur Heart J 28:2732–2737CrossRefPubMed
44.
Zurück zum Zitat Ouyang P, Saarel E, Bai Y, Luo C, Lv Q, Xu Y, Wang F, Fan C, Younoszai A, Chen Q, Tu X, Wang QK (2011) A de novo mutation in NKX2.5 associated with atrial septal defects, ventricular noncompaction, syncope and sudden death. Clin Chim Acta 412:170–175CrossRefPubMed Ouyang P, Saarel E, Bai Y, Luo C, Lv Q, Xu Y, Wang F, Fan C, Younoszai A, Chen Q, Tu X, Wang QK (2011) A de novo mutation in NKX2.5 associated with atrial septal defects, ventricular noncompaction, syncope and sudden death. Clin Chim Acta 412:170–175CrossRefPubMed
45.
Zurück zum Zitat Hoedemaekers YM, Caliskan K, Michels M, Frohn-Mulder I, van der Smagt JJ, Phefferkorn JE, Wessels MW, ten Cate FJ, Sijbrands EJ, Dooijes D, Majoor-Krakauer DF (2010) The importance of genetic counseling, DNA diagnostics, and cardiologic family screening in left ventricular noncompaction cardiomyopathy. Circ Cardiovasc Genet 3:232–239CrossRefPubMed Hoedemaekers YM, Caliskan K, Michels M, Frohn-Mulder I, van der Smagt JJ, Phefferkorn JE, Wessels MW, ten Cate FJ, Sijbrands EJ, Dooijes D, Majoor-Krakauer DF (2010) The importance of genetic counseling, DNA diagnostics, and cardiologic family screening in left ventricular noncompaction cardiomyopathy. Circ Cardiovasc Genet 3:232–239CrossRefPubMed
46.
Zurück zum Zitat Shan L, Makita N, Xing Y, Watanabe S, Futatani T, Ye F, Saito K, Ibuki K, Watanabe K, Hirono K, Uese K, Ichida F, Miyawaki T, Origasa H, Bowles NE, Towbin JA (2008) SCN5A variants in Japanese patients with left ventricular noncompaction and arrhythmia. Mol Genet Metab 93:468–474CrossRefPubMed Shan L, Makita N, Xing Y, Watanabe S, Futatani T, Ye F, Saito K, Ibuki K, Watanabe K, Hirono K, Uese K, Ichida F, Miyawaki T, Origasa H, Bowles NE, Towbin JA (2008) SCN5A variants in Japanese patients with left ventricular noncompaction and arrhythmia. Mol Genet Metab 93:468–474CrossRefPubMed
47.
Zurück zum Zitat Ronvelia D, Greenwood J, Platt J, Hakim S, Zaragoza MV (2012) Intrafamilial variability for novel TAZ gene mutation: Barth syndrome with dilated cardiomyopathy and heart failure in an infant and left ventricular noncompaction in his great-uncle. Mol Genet Metab 107:428–432CrossRefPubMedPubMedCentral Ronvelia D, Greenwood J, Platt J, Hakim S, Zaragoza MV (2012) Intrafamilial variability for novel TAZ gene mutation: Barth syndrome with dilated cardiomyopathy and heart failure in an infant and left ventricular noncompaction in his great-uncle. Mol Genet Metab 107:428–432CrossRefPubMedPubMedCentral
48.
Zurück zum Zitat Kapadia R, Choudhary P, Collins N, Celermajer D, Puranik R (2016) Left ventricular non-compaction in Holt–Oram syndrome. Heart Lung Circ 25:626–630CrossRefPubMed Kapadia R, Choudhary P, Collins N, Celermajer D, Puranik R (2016) Left ventricular non-compaction in Holt–Oram syndrome. Heart Lung Circ 25:626–630CrossRefPubMed
49.
Zurück zum Zitat Luedde M, Ehlermann P, Weichenhan D, Will R, Zeller R, Rupp S, Müller A, Steen H, Ivandic BT, Ulmer HE, Kern M, Katus HA, Frey N (2010) Severe familial left ventricular non-compaction cardiomyopathy due to a novel troponin T (TNNT2) mutation. Cardiovasc Res 86:452–460CrossRefPubMed Luedde M, Ehlermann P, Weichenhan D, Will R, Zeller R, Rupp S, Müller A, Steen H, Ivandic BT, Ulmer HE, Kern M, Katus HA, Frey N (2010) Severe familial left ventricular non-compaction cardiomyopathy due to a novel troponin T (TNNT2) mutation. Cardiovasc Res 86:452–460CrossRefPubMed
50.
Zurück zum Zitat Chang B, Nishizawa T, Furutani M, Fujiki A, Tani M, Kawaguchi M, Ibuki K, Hirono K, Taneichi H, Uese K, Onuma Y, Bowles NE, Ichida F, Inoue H, Matsuoka R, Miyawaki T, Noncompaction Study C (2011) Identification of a novel TPM1 mutation in a family with left ventricular noncompaction and sudden death. Mol Genet Metab 102:200–206CrossRefPubMed Chang B, Nishizawa T, Furutani M, Fujiki A, Tani M, Kawaguchi M, Ibuki K, Hirono K, Taneichi H, Uese K, Onuma Y, Bowles NE, Ichida F, Inoue H, Matsuoka R, Miyawaki T, Noncompaction Study C (2011) Identification of a novel TPM1 mutation in a family with left ventricular noncompaction and sudden death. Mol Genet Metab 102:200–206CrossRefPubMed
51.
Zurück zum Zitat Graham TP Jr, Jarmakani JM, Canent RV Jr, Morrow MN (1971) Left heart volume estimation in infancy and childhood. Reevaluation of methodology and normal values. Circulation 43:895–904CrossRefPubMed Graham TP Jr, Jarmakani JM, Canent RV Jr, Morrow MN (1971) Left heart volume estimation in infancy and childhood. Reevaluation of methodology and normal values. Circulation 43:895–904CrossRefPubMed
Metadaten
Titel
A mutant HCN4 channel in a family with bradycardia, left bundle branch block, and left ventricular noncompaction
verfasst von
Ryosuke Yokoyama
Koshi Kinoshita
Yukiko Hata
Masayoshi Abe
Kenta Matsuoka
Keiichi Hirono
Masanobu Kano
Makoto Nakazawa
Fukiko Ichida
Naoki Nishida
Toshihide Tabata
Publikationsdatum
18.01.2018
Verlag
Springer Japan
Erschienen in
Heart and Vessels / Ausgabe 7/2018
Print ISSN: 0910-8327
Elektronische ISSN: 1615-2573
DOI
https://doi.org/10.1007/s00380-018-1116-6

Weitere Artikel der Ausgabe 7/2018

Heart and Vessels 7/2018 Zur Ausgabe

Update Kardiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.