The HCN4 channel mutation D553N associated with bradycardia has a C-linker mediated gating defect

Cellular Physiology and Biochemistry

Volumn 30, Issue 5, 2012, Pages 1227-1240

  Nette, Michael F ^a   Zuzarte, Marylou ^a   Schlichthörl, Günter ^a   Klöcker, Nikolaj ^b   Decher, Niels ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Arrhythmia; C linker; CAMP; Cyclic nucleotide binding domain; D553N; HCN

Indexed keywords

CYCLIC AMP;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRADYCARDIA; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; CHANNEL GATING; CONTROLLED STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; LOSS OF FUNCTION MUTATION; MAMMAL CELL; NONHUMAN; OOCYTE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; XENOPUS LAEVIS;

MAMMALIA;

ANIMALS; BRADYCARDIA; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; ION CHANNEL GATING; MUSCLE PROTEINS; MUTATION; POTASSIUM CHANNELS; XENOPUS;

EID: 84867450920     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000343314     Document Type: Article

References (36)

1. Sanguinetti MC, Tristani-Firouzi M: hERG potassium channels and cardiac arrhythmia. Nature 2006;440:463-469.
2. Benson DW, Wang DW, Dyment M, Knilans TK, Fish FA, Strieper MJ, Rhodes TH, George AL Jr: Congenital sick sinus syndrome caused by recessive mutations in the cardiac sodium channel gene (SCN5A). J Clin Invest 2003;112:1019-1028. (Pubitemid 38056317)
3. Schulze-Bahr E, Neu A, Friederich P, Kaupp UB, Breithardt G, Pongs O, Isbrandt D: Pacemaker channel dysfunction in a patient with sinus node disease. J Clin Invest 2003;111:1537-1545. (Pubitemid 38063286)
4. Di Francesco D, Tortora P: Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 1991;351:145-147. (Pubitemid 21896552)
5. Zolles G, Klöcker N, Wenzel D, Weisser-Thomas J, Fleischmann BK, Röper J, Fakler B: Pacemaking by HCN channels requires interaction with phosphoinositides. Neuron 2006;52:1027-1036. (Pubitemid 44909413)
6. Zong X, Eckert C, Yuan H, Wahl-Schott C, Abicht H, Fang L, Li R, Mistrik P, Gerstner A, Much B, Baumann L, Michalakis S, Zeng R, Chen Z, Biel M: A novel mechanism of modulation of hyperpolarization-activated cyclic nucleotide-gated channels by Src kinase. J Biol Chem 2005;280:34224-34232. (Pubitemid 41443148)
7. Baruscotti M, Bucchi A, Viscomi C, Mandelli G, Consalez G, Gnecchi-Rusconi T, Montano N, Casali KR, Micheloni S, Barbuti A, Di Francesco D: Deep bradycardia and heart block caused by inducible cardiacspecific knockout of the pacemaker channel gene HCN4. Proc Natl Acad Sci USA 2011;108:1705-1710.
8. Stieber J, Herrmann S, Feil S, Loster J, Feil R, Biel M, Hofmann F, Ludwig A: The hyperpolarization-activated channel HCN4 is required for the generation of pacemaker action potentials in the embryonic heart. Proc Natl Acad Sci U S A 2003;100:15235-15240. (Pubitemid 37518045)
9. Ludwig A, Budde T, Stieber J, Moosmang S, Wahl C, Holthoff K, Langebartels A, Wotjak C, Munsch T, Zong X, Feil S, Feil R, Lancel M, Chien KR, Konnerth A, Pape HC, Biel M, Hofmann F: Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J 2003;22:216-224. (Pubitemid 36119427)
10. Ueda K, Nakamura K, Hayashi T, Inagaki N, Takahashi M, Arimura T, Morita H, Higashiuesato Y, Hirano Y, Yasunami M, Takishita S, Yamashina A, Ohe T, Sunamori M, Hiraoka M, Kimura A: Functional characterization of a trafficking-defective HCN4 mutation, D553N, associated with cardiac arrhythmia. J Biol Chem 2004;279:27194-27198. (Pubitemid 38812556)
11. Milanesi R, Baruscotti M, Gnecchi-Ruscone T, Di Francesco D: Familial sinus bradycardia associated with a mutation in the cardiac pacemaker channel. N Engl J Med 2006;354:151-157. (Pubitemid 43076712)
12. Schweizer PA, Duhme N, Thomas D, Becker R, Zehelein J, Draguhn A, Bruehl C, Katus HA, Koenen M: cAMP sensitivity of HCN pacemaker channels determines basal heart rate but is not critical for autonomic rate control. Circ Arrhythm Electrophysiol 2010;3:542-552.
13. Johnson JP Jr, Zagotta WN: The carboxyl-terminal region of cyclic nucleotide-modulated channels is a gating ring, not a permeation path. Proc Natl Acad Sci USA 2005;102:2742-2747. (Pubitemid 40299863)
14. Decher N, Chen J, Sanguinetti MC: Voltage-dependent gating of hyperpolarization-activated, cyclic nucleotide-gated pacemaker channels: molecular coupling between the S4-S5 and C-linkers. J Biol Chem 2004;279:13859-13865. (Pubitemid 38468918)
15. Craven KB, Olivier NB, Zagotta WN: C-terminal movement during gating in cyclic nucleotide-modulated channels. J Biol Chem 2008;283:14728-14738.
16. Craven KB, Zagotta WN: Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels. J Gen Physiol 2004;124:663-677. (Pubitemid 39628134)
17. Lin YC, Huang J, Kan H, Frisbee JC, Yu HG: Rescue of a trafficking defective human pacemaker channel via a novel mechanism: roles of Src, Fyn, and Yes tyrosine kinases. J Biol Chem 2009;284:30433-30440.
18. Claycomb WC, Lanson NA Jr, Stallworth BS, Egeland DB, Delcarpio JB, Bahinski A, Izzo NJ Jr: HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 1998;95:2979-2984. (Pubitemid 28135840)
19. Hardel N, Harmel N, Zolles G, Fakler B, Klöcker N: Recycling endosomes supply cardiac pacemaker channels for regulated surface expression. Cardiovasc Res 2008;79:52-60. (Pubitemid 351881930)
20. Much B, Wahl-Schott C, Zong X, Schneider A, Baumann L, Moosmang S, Ludwig A, Biel M: Role of subunit heteromerization and N-linked glycosylation in the formation of functional hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 2003;278:43781-43786. (Pubitemid 37346006)
21. Huang J, Huang A, Zhang Q, Lin YC, Yu HG: Novel mechanism for suppression of hyperpolarization-activated cyclic nucleotide-gated pacemaker channels by receptor-like tyrosine phosphatase-alpha. J Biol Chem 2008;283:29912-29919.
22. Li CH, Zhang Q, Teng B, Mustafa SJ, Huang JY, Yu HG: Src tyrosine kinase alters gating of hyperpolarizationactivated HCN4 pacemaker channel through Tyr531. Am J Physiol Cell Physiol 2008;294:C355-362.
23. Zagotta WN, Olivier NB, Black KD, Young EC, Olson R, Gouaux E: Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 2003;425:200-205. (Pubitemid 37150901)
24. Brandt MC, Endres-Becker J, Zagidullin N, Motloch LJ, Er F, Rottlaender D, Michels G, Herzig S, Hoppe UC: Effects of KCNE2 on HCN isoforms: distinct modulation of membrane expression and single channel properties. Am J Physiol Heart Circ Physiol 2009;297:H355-363.
25. Michels G, Er F, Khan I, Sudkamp M, Herzig S, Hoppe UC: Single-channel properties support a potential contribution of hyperpolarization-activated cyclic nucleotide-gated channels and If to cardiac arrhythmias. Circulation 2005;111:399-404. (Pubitemid 40204422)
26. Di Francesco D: Letter regarding article by Michels et al, "Single-channel properties support a potential contribution of hyperpolarization-activated cyclic nucleotide-gated channels and If to cardiac arrhythmias". Circulation 2005;112:e72; author reply e72-73.
27. Di Francesco D: Characterization of single pacemaker channels in cardiac sino-atrial node cells. Nature 1986;324:470-473. (Pubitemid 17184165)
28. f by cAMP in the rabbit sino-atrial node. J Physiol 1994;474:473-482. (Pubitemid 24060780)
29. Laish-Farkash A, Glikson M, Brass D, Marek-Yagel D, Pras E, Dascal N, Antzelevitch C, Nof E, Reznik H, Eldar M, Luria D: A novel mutation in the HCN4 gene causes symptomatic sinus bradycardia in moroccan jews. J Cardiovasc Electrophysiol 2010;21:1365-1372.
30. Nof E, Luria D, Brass D, Marek D, Lahat H, Reznik-Wolf H, Pras E, Dascal N, Eldar M, Glikson M: Point mutation in the HCN4 cardiac ion channel pore affecting synthesis, trafficking, and functional expression is associated with familial asymptomatic sinus bradycardia. Circulation 2007;116:463-470. (Pubitemid 47450254)
31. + channel. J Biol Chem 2006;281:12858-12864. (Pubitemid 43855379)
32. Varghese A, Tenbroek EM, Coles J Jr, Sigg DC: Endogenous channels in HEK cells and potential roles in HCN ionic current measurements. Prog Biophys Mol Biol 2006;90:26-37. (Pubitemid 41721042)
33. Arinsburg SS, Cohen IS, Yu HG: Constitutively active Src tyrosine kinase changes gating of HCN4 channels through direct binding to the channel proteins. J Cardiovasc Pharmacol 2006;47:578-586. (Pubitemid 44309677)
34. Xu X, Vysotskaya ZV, Liu Q, Zhou L: Structural basis for the cAMP-dependent gating in the human HCN4 channel. J Biol Chem 2010;285:37082-37091.
35. Chen J, Mitcheson JS, Tristani-Firouzi M, Lin M, Sanguinetti MC: The S4-S5 linker couples voltage sensing and activation of pacemaker channels. Proc Natl Acad Sci U S A 2001;98:11277-11282. (Pubitemid 32928719)
36. + channels. J Biol Chem 2002;277:18994-19000. (Pubitemid 34952462)