Atrial fibrillation and sinus node dysfunction in human ankyrin-B syndrome: A computational analysis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 9, 2013, Pages

  Wolf, Roseanne M ^a,d   Glynn, Patric ^a,b   Hashemi, Seyed ^e   Zarei, Keyan ^e   Mitchell, Colleen C ^d   Anderson, Mark E ^e   Mohler, Peter J ^a,c   Hund, Thomas J ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b The Ohio State University   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF IOWA   (United States)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

Ankyrin B; Arrhythmia (mechanisms); Atrial fibrillation; Sinus node disease

Indexed keywords

ANKYRIN; ANKYRIN B; CALCIUM CHANNEL L TYPE; REACTIVE OXYGEN METABOLITE; RYANODINE RECEPTOR; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; FIBROBLAST; HEART ATRIUM ARRHYTHMIA; HEART ATRIUM FIBRILLATION; HEART REPOLARIZATION; HEART VENTRICLE ARRHYTHMIA; HISTOLOGY; HUMAN; MALE; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; MOUSE; NERVE BLOCK; NONHUMAN; PRIORITY JOURNAL; REENTRY ARRHYTHMIA; SARCOPLASMIC RETICULUM; SINUS NODE; SINUS NODE DISEASE;

ANKYRIN-B; ARRHYTHMIA (MECHANISMS), ATRIAL FIBRILLATION; SINUS NODE DISEASE;

ACTION POTENTIALS; ANIMALS; ANKYRINS; ARRHYTHMIAS, CARDIAC; ATRIAL FIBRILLATION; CALCIUM CHANNELS, L-TYPE; COMPUTER SIMULATION; FIBROSIS; HEART ATRIA; HUMANS; MICE; MODELS, CARDIOVASCULAR; SINOATRIAL NODE; SODIUM-CALCIUM EXCHANGER; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84878618708     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00734.2012     Document Type: Article

References (46)

1. Bondarenko VE, Szigeti GP, Bett GC, Kim SJ, Rasmusson RL. Computer model of action potential of mouse ventricular myocytes. Am J Physiol Heart Circ Physiol 287: H1378-H1403, 2004.
2. 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 105: 1213-1222, 2009.
3. + channel (SCN5A) mutations and impaired cardiac pacemaking in sick sinus syndrome. Circ Res 107: 126-137, 2010.
4. Camelliti P, Borg TK, Kohl P. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc Res 65: 40-51, 2005.
5. Camors E, Mohler PJ, Bers DM, Despa S. Ankyrin-B reduction enhances Ca spark-mediated SR Ca release promoting cardiac myocyte arrhythmic activity. J Mol Cell Cardiol 52: 1240-1248, 2012.
6. Christensen MD, Dun W, Boyden PA, Anderson ME, Mohler PJ, Hund TJ. Oxidized calmodulin kinase II regulates conduction following myocardial infarction: a computational analysis. PLoS Comput Biol 5: e1000583, 2009.
7. Courtemanche M, Ramirez RJ, Nattel S. Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. Am J Physiol Heart Circ Physiol 275: H301-H321, 1998.
8. Cunha SR, Bhasin N, Mohler PJ. Targeting and stability of Na/Ca exchanger 1 in cardiomyocytes requires direct interaction with the membrane adaptor ankyrin-B. J Biol Chem 282: 4875-4883, 2007.
9. Cunha SR, Hund TJ, Hashemi S, Voigt N, Li N, Wright P, Koval O, Li J, Gudmundsson H, Gumina RJ, Karck M, Schott J, Probst V, Le Marec H, Anderson ME, Dobrev D, Wehrens XH, Mohler PJ. Defects in ankyrin-based membrane protein targeting pathways underlie atrial fibrillation. Circulation 124: 1212-1222, 2011.
10. De Maziere AM, van Ginneken AC, Wilders R, Jongsma HJ, Bouman LN. Spatial and functional relationship between myocytes and fibroblasts in the rabbit sinoatrial node. J Mol Cell Cardiol 24: 567-578, 1992.
11. DeGrande S, Nixon D, Koval O, Curran JW, Wright P, Wang Q, Kashef F, Chiang D, Li N, Wehrens XH, Anderson ME, Hund TJ, Mohler PJ. CaMKII inhibition rescues pro-arrhythmic phenotypes in model of human ankyrin-B syndrome. Heart Rhythm 9: 2034-2041, 2012.
12. Dobrzynski H, Boyett MR, Anderson RH. New insights into pacemaker activity: promoting understanding of sick sinus syndrome. Circulation 115: 1921-1932, 2007.
13. Dobrzynski H, Li J, Tellez J, Greener ID, Nikolski VP, Wright SE, Parson SH, Jones SA, Lancaster MK, Yamamoto M, Honjo H, Takagishi Y, Kodama I, Efimov IR, Billeter R, Boyett MR. Computer three-dimensional reconstruction of the sinoatrial node. Circulation 111: 846-854, 2005.
14. Friedrichs K, Baldus S, Klinke A. Fibrosis in atrial fibrillation-role of reactive species and MPO. Front Physiol 3: 214, 2012.
15. Glukhov AV, Fedorov VV, Anderson ME, Mohler PJ, Efimov IR. Functional anatomy of the murine sinus node: high-resolution optical mapping of ankyrin-B heterozygous mice. Am J Physiol Heart Circ Physiol 299: H482-H491, 2010.
16. 2+ model: sinus rhythm and chronic atrial fibrillation. Circ Res 109: 1055-1066, 2011.
17. Hund TJ, Decker KF, Kanter E, Mohler PJ, Boyden PA, Schuessler RB, Yamada KA, Rudy Y. Role of activated CaMKII in abnormal calcium homeostasis and INa remodeling after myocardial infarction: Insights from mathematical modeling. J Mol Cell Cardiol 45: 420-428, 2008.
18. Hund TJ, Kucera JP, Otani NF, Rudy Y. Ionic charge conservation and long-term steady state in the Luo-Rudy dynamic model of the cardiac cell. Biophys J 81: 3324-3331, 2001.
19. Hund TJ, Wright PJ, Dun W, Snyder JS, Boyden PA, Mohler PJ. Regulation of the ankyrin-B-based targeting pathway following myocardial infarction. Cardiovasc Res 81: 742-749, 2009.
20. Joyner RW, Ramon F, Morre JW. Simulation of action potential propagation in an inhomogeneous sheet of coupled excitable cells. Circ Res 36: 654-661, 1975.
21. Kamkin A, Kiseleva I, Isenberg G. Activation and inactivation of a non-selective cation conductance by local mechanical deformation of acutely isolated cardiac fibroblasts. Cardiovasc Res 57: 793-803, 2003.
22. Kashef F, Li J, Wright P, Snyder J, Suliman F, Kilic A, Higgins RS, Anderson ME, Binkley PF, Hund TJ, Mohler PJ. Ankyrin-B in heart failure: Identification of a new component of metazoan cardioprotection. J Biol Chem 287: 30268-30281, 2012.
23. Kharche S, Yu J, Lei M, Zhang H. A mathematical model of action potentials of mouse sinoatrial node cells with molecular bases. Am J Physiol Heart Circ Physiol 301: H945-H963, 2011.
24. Kohl P, Kamkin AG, Kiseleva IS, Noble D. Mechanosensitive fibroblasts in the sino-atrial node region of rat heart: interaction with cardiomyocytes and possible role. Exp Physiol 79: 943-956, 1994.
25. Krogh-Madsen T, Abbott GW, Christini DJ. Effects of electrical and structural remodeling on atrial fibrillation maintenance: a simulation study. PLoS Comput Biol 8: e1002390, 2012.
26. + channel current. Biophys J 95: 951-977, 2008.
27. Le Scouarnec S, Bhasin N, Vieyres C, Hund TJ, Cunha SR, Koval O, Marionneau C, Chen B, Wu Y, Demolombe S, Song LS, Le Marec H, Probst V, Schott JJ, Anderson ME, Mohler PJ. Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci USA 105: 15617-15622, 2008.
28. Lee JM, Kalman JM. Sinus node dysfunction and atrial fibrillation: two sides of the same coin? Europace 15: 161-162, 2012.
29. Letavernier E, Zafrani L, Perez J, Letavernier B, Haymann JP, Baud L. The role of calpains in myocardial remodelling and heart failure. Cardiovasc Res 96: 38-45, 2012.
30. Liu J, Dobrzynski H, Yanni J, Boyett MR, Lei M. Organisation of the mouse sinoatrial node: structure and expression of HCN channels. Cardiovasc Res 73: 729-738, 2007.
31. Mohler PJ, Davis JQ, Bennett V. Ankyrin-B coordinates the Na/K ATPase, Na/Ca exchanger, and InsP3 receptor in a cardiac T-tubule/SR microdomain. PLoS Biol 3: e423, 2005.
32. Mohler PJ, Healy JA, Xue H, Puca AA, Kline CF, Allingham RR, Kranias EG, Rockman HA, Bennett V. Ankyrin-B syndrome: enhanced cardiac function balanced by risk of cardiac death and premature senescence. PLoS One 2: e1051, 2007.
33. Mohler PJ, Le Scouarnec S, Denjoy I, Lowe JS, Guicheney P, Caron L, Driskell IM, Schott JJ, Norris K, Leenhardt A, Kim RB, Escande D, Roden DM. Defining the cellular phenotype of "ankyrin-B syndrome" variants: human ANK2 variants associated with clinical phenotypes display a spectrum of activities in cardiomyocytes. Circulation 115: 432-441, 2007.
34. Mohler PJ, Schott JJ, Gramolini AO, Dilly KW, Guatimosim S, duBell WH, Song LS, Haurogne K, Kyndt F, Ali ME, Rogers TB, Lederer WJ, Escande D, Le Marec H, Bennett V. Ankyrin-B mutation causes type 4 long-QT cardiac arrhythmia and sudden cardiac death. Nature 421: 634-639, 2003.
35. Mohler PJ, Splawski I, Napolitano C, Bottelli G, Sharpe L, Timothy K, Priori SG, Keating MT, Bennett V. A cardiac arrhythmia syndrome caused by loss of ankyrin-B function. Proc Natl Acad Sci USA 101: 9137-9142, 2004.
36. Morita N, Sovari AA, Xie Y, Fishbein MC, Mandel WJ, Garfinkel A, Lin SF, Chen PS, Xie LH, Chen F, Qu Z, Weiss JN, Karagueuzian HS. Increased susceptibility of aged hearts to ventricular fibrillation during oxidative stress. Am J Physiol Heart Circ Physiol 297: H1594-H1605, 2009.
37. 2+ channels. Cell 102: 89-97, 2000.
38. Rohr S. Myofibroblasts in diseased hearts: new players in cardiac arrhythmias? Heart Rhythm 6: 848-856, 2009.
39. Rudy Y, Silva JR. Computational biology in the study of cardiac ion channels and cell electrophysiology. Q Rev Biophys 39: 57-116, 2006.
40. Schott JJ, Charpentier F, Peltier S, Foley P, Drouin E, Bouhour JB, Donnelly P, Vergnaud G, Bachner L, Moisan JP, Le Marec H, Paschal O. Mapping of a gene for long QT syndrome to chromosome 4q25-27. Am J Hum Genet 57: 1114-1122, 1995.
41. Smith S, Curran J, Hund TJ, Mohler PJ. Defects in cytoskeletal signaling pathways, arrhythmia, and sudden cardiac death. Front Physiol 3: 122, 2012.
42. Swaminathan PD, Purohit A, Soni S, Voigt N, Singh MV, Glukhov AV, Gao Z, He JB, Luczak ED, Joiner ML, Kutschke W, Yang J, Donahue JK, Weiss RM, Grumbach IM, Ogawa M, Chen PS, Efimov IR, Dobrev D, Mohler PJ, Hund TJ, Anderson ME. Oxidized CaMKII causes sinus node dysfunction. J Clin Invest 121: 3277-3288, 2011.
43. Weiss JN, Nivala M, Garfinkel A, Qu Z. Alternans and arrhythmias: from cell to heart. Circ Res 108: 98-112, 2011.
44. Wolf RM, Mitchell CC, Christensen MD, Mohler PJ, Hund TJ. Defining new insight into atypical arrhythmia: a computational model of ankyrin-B-syndrome. Am J Physiol Heart Circ Physiol 299: H1505-H1514, 2010.
45. Workman AJ, Kane KA, Rankin AC. The contribution of ionic currents to changes in refractoriness of human atrial myocytes associated with chronic atrial fibrillation. Cardiovasc Res 52: 226-235, 2001.
46. 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 95: 4469-4480, 2008.