Disease and region-related cardiac fibroblast potassium current variations and potential functional significance

Cardiovascular Research

Volumn 102, Issue 3, 2014, Pages 487-496

  Wu, Chia Tung ^a,b   Qi, Xiao Yan ^a   Huang, Hai ^a   Naud, Patrice ^a   Dawson, Kristin ^a,c   Yeh, Yung Hsin ^b   Harada, Masahide ^a,d   Kuo, Chi Tai ^b   Nattel, Stanley ^a,c  

^a MONTREAL HEART INSTITUTE   (Canada)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^c MCGILL UNIVERSITY   (Canada)

^d HAMAMATSU MEDICAL CENTER   (Japan)

Author keywords

Congestive heart failure; Fibroblast; Ionic channel; Proliferation; Remodelling

Indexed keywords

MESSENGER RNA; PAXILLINE; POTASSIUM CHANNEL KCA1.1; POTASSIUM CHANNEL KV1.5; POTASSIUM CHANNEL KV4.3; THYMIDINE; UNCLASSIFIED DRUG; TETRYLAMMONIUM; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARRHYTHMOGENESIS; ARTICLE; CELL PROLIFERATION; CONGESTIVE HEART FAILURE; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HEART ATRIUM FIBRILLATION; HEART MUSCLE FIBROSIS; IC 50; MALE; MEMBRANE STEADY POTENTIAL; NONHUMAN; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; VOLTAGE CLAMP TECHNIQUE; ANIMAL; ATRIAL FIBRILLATION; COMPLICATION; DOG; FIBROSIS; HEART FAILURE; HEART MUSCLE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ATRIAL FIBRILLATION; DOGS; FIBROBLASTS; FIBROSIS; HEART FAILURE; MALE; MYOCARDIUM; POTASSIUM CHANNELS, VOLTAGE-GATED; TETRAETHYLAMMONIUM COMPOUNDS;

EID: 84901475702     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu055     Document Type: Article

References (42)

1. Nag A. Study of non-muscle cells of the adult mammalian heart: A fine structural analysis and distribution. Cytobios 1980;28: 41-61.
2. Pedrotty DM, Klinger RY, Kirkton RD, Bursac N. Cardiac fibroblast paracrine factors alter impulse conduction and ion channel expression of neonatal rat cardiomyocytes. Cardiovasc Res 2009;83: 688-697.
3. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 2005;65: 40-51.
4. Yue L, Xie J, Nattel S. Molecular determinants of cardiac fibroblast electrical function and therapeutic implications for atrial fibrillation. Cardiovasc Res 2011;89: 744-753.
5. Burstein B, Comtois P, Michael G, Nishida K, Villeneuve L, Yeh YH, Nattel S. Changes in connexin expression and the atrial fibrillation substrate in congestive heart failure. Circ Res 2009;105: 1213-1222.
6. Kawara T, Derksen R, de Groot JR, Coronel R, Tasseron S, Linnenbank AC, Hauer RN, Kirkels H, Janse MJ, de Bakker JM. Activation delay after premature stimulation in chronically diseased human myocardium relates to the architecture of interstitial fibrosis. Circulation 2001;104: 3069-3075.
7. Camelliti P, Green CR, LeGrice I, Kohl P. Fibroblast network in rabbit sinoatrial node: Structural and functional identification of homogeneous and heterogeneous cell coupling. Circ Res 2004;94: 828-835.
8. Gaudesius G, Miragoli M, Thomas SP, Rohr S. Coupling of cardiac electrical activity over extended distances by fibroblasts of cardiac origin. Circ Res 2003;93: 421-428.
9. Kohl P, Camelliti P. Fibroblast-myocyte connections in the heart. Heart Rhythm 2012;9: 461-464.
10. Kamkin A, Kiseleva I, Isenberg G, Wagner KD, Günther J, Theres H, Scholz H. Cardiac fibroblasts and the mechano-electric feedback mechanism in healthy and diseased hearts. Prog Biophys Mol Biol 2003;82: 111-120.
11. Kamkin A, Kiseleva I, Lozinsky I, Scholz H. Electrical interaction of mechanosensitive fibroblasts and myocytes in the heart. Basic Res Cardiol 2005;100: 337-345.
12. 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: 1-10.
13. Chilton L, Ohya S, Freed D, George E, Drobic V, Giles WR. K+ currents regulate the restingmembrane potential, proliferation, and contractile responses in ventricular fibroblasts and myofibroblasts. Am J Physiol Heart Circ Physiol 2005;288: H2931-H2939.
14. Hanna N, Cardin S, Leung TK, Nattel S. Differences in atrial versus ventricular remodeling in dogs with ventricular tachypacing-induced congestive heart failure. Cardiovasc Res 2004;63: 236-244.
15. Burstein B, Libby E, Calderone A, Nattel S. Differential behaviors of atrial versus ventricular fibroblasts: A potential role for platelet-derived growth factor in atrial-ventricular remodeling differences. Circulation 2008;117: 1630-1641.
16. Li D, Fareh S, Leung TK, Nattel S. Promotion of atrial fibrillation by heart failure in dogs: Atrial remodeling of a different sort. Circulation 1999;100: 87-95.
17. Bachmann A, Gutcher I, Kopp K, Brendel J, Bosch RF, Busch AE, Gö gelein H. Characterization of a novel Kv1.5 channel blocker in Xenopus oocytes, CHO cells, human and rat cardiomyocytes. Naunyn Schmiedebergs Arch Pharmacol 2001;364: 472-478.
18. Li G, CheungDW. Effects of paxilline on K+ channels in rat mesenteric arterial cells. Eur J Pharmacol 1999;372: 103-107.
19. Sanchez M, McManus OB. Paxilline inhibition of the alpha-subunit of the highconductance calcium-activated potassium channel. Neuropharmacology 1996;35: 963-968.
20. Dawson K, Wu CT, Qi XY, Nattel S. Congestive heart failure effects on atrial fibroblast phenotype: Differences between freshly-isolated and cultured cells. PLoS ONE 2012;7: E52032.
21. Shibukawa Y, Chilton EL, MacCannell KA, Clark RB, Giles WR. K+ currents activated by depolarization in cardiac fibroblasts. Biophys J 2005;88: 3924-3935.
22. Tabibiazar R, Wagner RA, Liao A, Quertermous T. Transcriptional profiling of the heart reveals chamber-specific gene expression patterns. Circ Res 2003;93: 1193-1201.
23. Ellinghaus P, Scheubel RJ, Dobrev D, Ravens U, Holtz J, Huetter J, Nielsch U, Morawietz H. Comparing the global mRNA expression profile of human atrial and ventricular myocardium with high-density oligonucleotide arrays. J Thorac Cardiovasc Surg 2005;129: 1383-1390.
24. Gaborit N, Le Bouter S, Szuts V, Varro A, Escande D, Nattel S, Demolombe S. Regional and tissue specific transcript signatures of ion channel genes in the non-diseased human heart. J Physiol 2007;582: 675-693.
25. Kardami E, Fandrich RR. Basic fibroblast growth factor in atria and ventricles of the vertebrate heart. J Cell Biol 1989;109: 1865-1875.
26. Goldsmith EC, Hoffman A, Morales MO, Potts JD, Price RL, McFadden A, Rice M, Borg TK. Organization of fibroblasts in the heart. Dev Dyn 2004;230: 787-794.
27. Rook MB, van Ginneken AC, de Jonge B, el Aoumari A, Gros D, Jongsma HJ. Differences in gap junction channels between cardiac myocytes, fibroblasts, and heterologous pairs. Am J Physiol 1992;263: C959-C977.
28. Vasquez C, Mohandas P, Louie KL, Benamer N, Bapat AC, Morley GE. Enhanced fibroblast-myocyte interactions in response to cardiac injury. Circ Res 2010;107: 1011-1020.
29. Xie Y, Garfinkel A, Camelliti P, Kohl P, Weiss JN, Qu Z. Effects of fibroblast-myocyte coupling on cardiac conduction and vulnerability to reentry: A computational study. Heart Rhythm 2009;6: 1641-1649.
30. Thompson SA, Copeland CR, Reich DH, Tung L. Mechanical coupling between myofibroblasts and cardiomyocytes slows electric conduction in fibrotic cell monolayers. Circulation 2011;123: 2083-2093.
31. Miragoli M, Salvarani N, Rohr S. Myofibroblasts induce ectopic activity in cardiac tissue. Circ Res 2007;101: 755-758.
32. Zlochiver S, Munoz V, Vikstrom KL, Taffet SM, Berenfeld O, Jalife J. Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophys J 2008;95: 4469-4480.
33. JacquemetV, Henriquez CS. Loading effect of fibroblast-myocyte coupling on resting potential, impulse propagation, and repolarization: Insights from a microstructure model. Am J Physiol Heart Circ Physiol 2008;294: H2040-H2052.
34. Sachse FB, Moreno AP, Seemann G, Abildskov JA. A model of electrical conduction in cardiac tissue including fibroblasts. Ann Biomed Eng 2009;37: 874-889.
35. Xie Y, Garfinkel A, Weiss JN, Qu Z. Cardiac alternans induced by fibroblast-myocyte coupling: Mechanistic insights from computational models. Am J Physiol Heart Circ Physiol 2009;297: H775-H784.
36. Maleckar MM, Greenstein JL, Giles WR, Trayanova NA. Electrotonic coupling between human atrial myocytes and fibroblasts alters myocyte excitability and repolarization. Biophys J 2009;97: 2179-2190.
37. Ashihara T, Haraguchi R, Nakazawa K, Namba T, Ikeda T, Nakazawa Y, Ozawa T, Ito M, Horie M, Trayanova NA. The role of fibroblasts in complex fractionated electrograms during persistent/permanent atrial fibrillation: Implications for electrogram-based catheter ablation. Circ Res 2012;110: 275-284.
38. Tomasek JJ, Abbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodeling. Nat Rev Mol Cell Biol 2002;3: 349-363.
39. Failli P, TescoG, Ruocco C, Ginestroni A, Amaducci L, Giotti A, Sorbi S. The effect of tetraethylammonium on intracellular calcium concentration in Alzheimer's disease fibroblasts with APP, S182 and E5-1 missense mutations. Neurosci Lett 1996;208: 216-218.
40. Etcheberrigaray R, Ito E, Oka K, Tofel-Grehl B, Gibson GE, Alkon DL. Potassium channel dysfunction in fibroblasts identifies patients with Alzheimer disease. Proc Natl Acad Sci USA 1993;90: 8209-8213.
41. Hu X, Laragione T, Sun L, Koshy S, Jones KR, Ismailov II, Yotnda P, Horrigan FT, Gulko PS, Beeton C. KCa1.1 potassium channels regulate key proinflammatory and invasive properties of fibroblast-like synoviocytes in rheumatoid arthritis. J Biol Chem 2012;287: 4014-4022.
42. He ML, Liu WJ, Sun HY, WuW, Liu J, Tse HF, Lau CP, Li GR. Effects of ion channels on proliferation in cultured human cardiac fibroblasts. J Mol Cell Cardiol 2011;51: 198-206.