Fibroblast proliferation alters cardiac excitation conduction and contraction: A computational study

Journal of Zhejiang University: Science B

Volumn 15, Issue 3, 2014, Pages 225-242

  Zhan, He Qing ^a   Xia, Ling ^a   Shou, Guo Fa ^a   Zang, Yun Liang ^a   Liu, Feng ^b   Crozier, Stuart ^b  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Cardiac model; Electromechanics; Fibroblast proliferation

Indexed keywords

CALCIUM;

ACTION POTENTIAL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; EXCITATION; EXCITATION CONTRACTION COUPLING; FIBROBLAST; FINITE ELEMENT ANALYSIS; HEART CONDUCTION; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; HUMAN CELL; MEMBRANE CONDUCTANCE; NERVE BLOCK; PRIORITY JOURNAL; REPOLARIZATION; STIMULUS; TISSUE LEVEL;

ACTION POTENTIALS; COMPUTER SIMULATION; FIBROBLASTS; FINITE ELEMENT ANALYSIS; HEART CONDUCTION SYSTEM; HUMANS; MODELS, CARDIOVASCULAR; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC;

EID: 84897071086     PISSN: 16731581     EISSN: 18621783     Source Type: Journal    
DOI: 10.1631/jzus.B1300156     Document Type: Article

References (60)

1. Antoni, M.L., Mollema, S.A., Delgado, V., et al., 2010. Prognostic importance of strain and strain rate after acute myocardial infarction. Eur. Heart J., 31(13):1640-1647. [doi:10.1093/eurheartj/ehq105]
2. Assomull, R.G., Prasad, S.K., Lyne, J., et al., 2006. Cardiovascular magnetic resonance, fibrosis, and prognosis in dilated cardiomyopathy. J. Am. Coll. Cardiol., 48(10): 1977-1985. [doi:10.1016/j.jacc.2006.07.049] (Pubitemid 44738448)
3. Banerjee, I., Fuseler, J.W., Price, R.L., et al., 2007. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am. J. Physiol. Heart Circ. Physiol., 293(3):H1883-H1891. [doi:10.1152/ajpheart.00514.2007] (Pubitemid 47367239)
4. Berry, M.F., Engler, A.J., Woo, Y.J., et al., 2006. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol., 290 (6):H2196-H2203. [doi:10.1152/ajpheart.01017. 2005] (Pubitemid 43846045)
5. Beuckelmann, D.J., Nābauer, M., Erdmann, E., 1992. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation, 85(3):1046-1055. [doi:10.1161/01.CIR.85.3.1046]
6. Biernacka, A., Frangogiannis, N.G., 2011. Aging and cardiac fibrosis. Aging Dis., 2(2):158-173.
7. Brown, R.A., Prajapati, R., McGrouther, D.A., et al., 1998. Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J. Cell. Physiol., 175(3):323-332.[doi:10. 1002/(SICI)1097-4652(199806)175:3〈323::AID-JCP10〉3.0.CO;2-6] (Pubitemid 28198212)
8. Camelliti, P., Borg, T.K., Kohl, P., 2005. Structural and functional characterisation of cardiac fibroblasts. Cardiovasc. Res., 65(1):40-51. [doi:10.1016/j.cardiores.2004.08.020] (Pubitemid 40038477)
9. Carusi, A., Burrage, K., Rodriguez, B., 2012. Bridging experiments, models and simulations: an integrative approach to validation in computational cardiac electrophysiology. Am. J. Physiol. Heart Circ. Physiol., 303(2):H144-H155. [doi:10.1152/ajpheart.01151.2011]
10. Cherry, E.M., Fenton, F.H., 2011. Effects of boundaries and geometry on the spatial distribution of action potential duration in cardiac tissue. J. Theor. Biol., 285(1):164-176. [doi:10.1016/j.jtbi.2011.06.039]
11. + currents regulate the resting membrane potential, proliferation, and contractile responses in ventricular fibroblasts and myofibroblasts. Am. J. Physiol. Heart Circ. Physiol., 288(6):H2931-H2939. [doi:10.1152/ajpheart.01220.2004]
12. Clayton, R.H., Bernus, O., Cherry, E.M., et al., 2011. Models of cardiac tissue electrophysiology: progress, challenges and open questions. Prog. Biophys. Mol. Biol., 104(1-3): 22-48. [doi:10.1016/j.pbiomolbio.2010.05.008]
13. Conrad, C.H., Brooks, W.W., Hayes, J.A., et al., 1995. Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation, 91(1):161-170. [doi:10.1161/01.CIR.91.1.161]
14. de Bakker, J.M., van Rijen, H.M., 2006. Continuous and discontinuous propagation in heart muscle. J. Cardiovasc. Electrophysiol., 17(5):567-573. [doi:10.1111/j.1540-8167.2006.00367.x]
15. Eastwood, M., McGrouther, D.A., Brown, R.A., 1998. Fibroblast responses to mechanical forces. Proc. Inst. Mech. Eng. H J. Eng. Med., 212(2):85-92. [doi:10.1243/0954411981533854] (Pubitemid 128769985)
16. 2+ handling and interval-force relations: a modelling study. Phil. Trans. R. Soc. A Math. Phys. Eng. Sci., 364(1842):1107-1133. [doi:10.1098/rsta.2006.1758]
17. Jacquemet, V., Henriquez, C.S., 2008. Loading effect of fibroblast-myocyte coupling on resting potential, impulse propagation, and repolarization: insights from a microstructure model. Am. J. Physiol. Heart Circul. Physiol., 294(5):H2040-H2052. [doi:10.1152/ajpheart.01298.2007]
18. John, B.T., Tamarappoo, B.K., Titus, J.L., et al., 2004. Global remodeling of the ventricular interstitium in idiopathic myocardial fibrosis and sudden cardiac death. Heart Rhythm, 1(2):141-149. [doi:10.1016/j.hrthm.2004.02. 021] (Pubitemid 38885657)
19. Kamkin, A., Kiseleva, I., Wagner, K.D., et al., 1999. Mechanically induced potentials in fibroblasts from human right atrium. Exp. Physiol., 84(2):347-356. [doi:10.1111/j.1469-445X.1999.01794.x] (Pubitemid 29150023)
20. Kerckhoffs, R.C.P., Healy, S.N., Usyk, T.P., et al., 2006. Computational methods for cardiac electromechanics. Proc. IEEE, 94(4):769-783. [doi:10.1109/JPROC.2006.871772]
21. Kerckhoffs, R.C.P., Omens, J.H., McCulloch, A.D., et al., 2010. Ventricular dilation and electrical dyssynchrony synergistically increase regional mechanical nonuniformity but not mechanical dyssynchrony: a computational model. Circ. Heart Fail., 3(4):528-536. [doi:10.1161/ CIRCHEARTFAILURE.109.862144]
22. Kohl, P., 2003. Heterogeneous cell coupling in the heart: an electrophysiological role for fibroblasts. Circul. Res., 93(5):381-383. [doi:10.1161/01.RES.0000091364.90121.0C93/5/381] (Pubitemid 37100000)
23. Kohl, P., Kamkin, A.G., Kiseleva, I.S., et al., 1994. Mechanosensitive fibroblasts in the sino-atrial node region of rat heart: interaction with cardiomyocytes and possible role. Exp. Physiol., 79(6):943-956. (Pubitemid 2163414)
24. Kuijpers, N.H., Hermeling, E., Bovendeerd, P.H., et al., 2012. Modeling cardiac electromechanics and mechanoelectrical coupling in dyssynchronous and failing hearts: insight from adaptive computer models. J. Cardiovasc. Transl. Res., 5(2):159-169. [doi:10.1007/s12265-012-9346-y]
25. MacCannell, K.A., Bazzazi, H., Chilton, L., et al., 2007. A mathematical model of electrotonic interactions between ventricular myocytes and fibroblasts. Biophys. J., 92(11): 4121-4132. [doi:10.1529/biophysj.106.101410] (Pubitemid 46910596)
26. Maleckar, M.M., Greenstein, J.L., Giles, W.R., et al., 2009. Electrotonic coupling between human atrial myocytes and fibroblasts alters myocyte excitability and repolarization. Biophys. J., 97(8):2179-2190. [doi:10.1016/j.bpj.2009.07.054]
27. Manabe, I., Shindo, T., Nagai, R., 2002. Gene expression in fibroblasts and fibrosis: involvement in cardiac hypertrophy. Circul. Res., 91(12):1103-1113. [doi:10.1161/01.RES.0000046452.67724.B8] (Pubitemid 36076358)
28. Miragoli, M., Gaudesius, G., Rohr, S., 2006. Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circul. Res., 98(6):801-810. [doi:10.1161/01.RES.0000214537.44195.A3]
29. Miragoli, M., Salvarani, N., Rohr, S., 2007. Myofibroblasts induce ectopic activity in cardiac tissue. Circul. Res., 101(8): 755-758. [doi:10.1161/CIRCRESAHA.107.160549] (Pubitemid 350287189)
30. Nash, M.P., Panfilov, A.V., 2004. Electromechanical model of excitable tissue to study reentrant cardiac arrhythmias. Prog. Biophys. Mol. Biol., 85(2-3):501-522. [doi:10.1016/j.pbiomolbio.2004.01.016] (Pubitemid 38629923)
31. Nickerson, D., Smith, N., Hunter, P., 2005. New developments in a strongly coupled cardiac electromechanical model. Europace, 7(Suppl. 2):118-127. [doi:10.1016/j.eupc.2005.04.009]
32. Niederer, S.A., Smith, N.P., 2008. An improved numerical method for strong coupling of excitation and contraction models in the heart. Prog. Biophys. Mol. Biol., 96(1-3): 90-111. [doi:10.1016/j.pbiomolbio.2007.08.001] (Pubitemid 351635620)
33. Niederer, S.A., Smith, N.P., 2009. The role of the Frank- Starling law in the transduction of cellular work to whole organ pump function: a computational modeling analysis. PLoS Comput. Biol., 5(4):e1000371. [doi:10.1371/journal. pcbi.1000371]
34. Niederer, S.A., Hunter, P.J., Smith, N.P., 2006. A quantitative analysis of cardiac myocyte relaxation: a simulation study. Biophys. J., 90(5):1697-1722. [doi:10.1529/biophysj.105.069534]
35. Niederer, S.A., Plank, G., Chinchapatnam, P., et al., 2011. Length-dependent tension in the failing heart and the efficacy of cardiac resynchronization therapy. Cardiovasc. Res., 89(2):336-343. [doi:10.1093/cvr/ cvq318]
36. Pellman, J., Lyon, R.C., Sheikh, F., 2010. Extracellular matrix remodeling in atrial fibrosis: mechanisms and implications in atrial fibrillation. J. Mol. Cell. Cardiol., 48(3): 461-467. [doi:10.1016/j.yjmcc.2009. 09.001]
37. Rice, J.J., Winslow, R.L., Hunter, W.C., 1999. Comparison of putative cooperative mechanisms in cardiac muscle: length dependence and dynamic responses. Am. J. Physiol. Heart Circul. Physiol., 45(5):H1734-H1754. (Pubitemid 29246563)
38. Rook, M.B., van Ginneken, A.C.G., de Jonge, B.E., et al., 1992. Differences in gap junction channels between cardiac myocytes, fibroblasts, and heterologous pairs. Am. J. Physiol. Cell Physiol., 263(5):C959-C977.
39. Rossi, M.A., 2001. Connective tissue skeleton in the normal left ventricle and in hypertensive left ventricular hypertrophy and chronic chagasic myocarditis. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res., 7(4):820-832. (Pubitemid 32691767)
40. Sachse, F.B., Moreno, A.P., Abildskov, J.A., 2008. Electrophysiological modeling of fibroblasts and their interaction with myocytes. Annals Biomed. Eng., 36(1): 41-56. [doi:10.1007/s10439-007-9405-8] (Pubitemid 50002703)
41. Sachse, F.B., Moreno, A.P., Seemann, G., et al., 2009. A model of electrical conduction in cardiac tissue including fibroblasts. Ann. Biomed. Eng., 37(5):874-889. [doi:10.1007/s10439-009-9667-4]
42. + currents activated by depolarization in cardiac fibroblasts. Biophys. J., 88(6):3924-3935. [doi:10.1529/biophysj.104.054429]
43. Shou, G.F., Xia, L., Jiang, M.F., et al., 2011. Magnetocardiography simulation based on an electrodynamic heart model. IEEE Trans. Magn., 47(9):2224-2230. [doi:10.1109/TMAG.2011.2143423]
44. Spach, M.S., Heidlage, J.F., Dolber, P.C., et al., 2007. Mechanism of origin of conduction disturbances in aging human atrial bundles: experimental and model study. Heart Rhythm, 4(2):175-185. [doi:10.1016/j.hrthm.2006.10.023] (Pubitemid 46158701)
45. Tanaka, K., Zlochiver, S., Vikstrom, K.L., et al., 2007. Spatial distribution of fibrosis governs fibrillation wave dynamics in the posterior left atrium during heart failure. Circul. Res., 101(8):839-847. [doi:10.1161/CIRCRESAHA.107.153858] (Pubitemid 350287199)
46. ten Tusscher, K.H.W.J., Panfilov, A.V., 2003. Influence of nonexcitable cells on spiral breakup in two-dimensional and three-dimensional excitable media. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 68(6):062902. [doi:10.1103/PhysRevE.68.062902]
47. ten Tusscher, K.H.W.J., Panfilov, A.V., 2005. Wave propagation in excitable media with randomly distributed obstacles. Multiscale Model. Simul., 3(2):265-282. [doi:10.1137/030602654] (Pubitemid 40951972)
48. ten Tusscher, K.H.W.J., Panfilov, A.V., 2007. Influence of diffuse fibrosis on wave propagation in human ventricular tissue. Europace, 9(Suppl. 6):vi38-vi45. [doi:10.1093/europace/eum206]
49. ten Tusscher, K.H.W.J., Noble, D., Noble, P.J., et al., 2004. A model for human ventricular tissue. Am. J. Physiol. Heart Circ. Physiol., 286(4):H1573-H1589. [doi:10.1152/ajpheart.00794.200300794.2003] (Pubitemid 38381170)
50. Trayanova, N.A., 2011. Whole-heart modeling: applications to cardiac electrophysiology and electromechanics. Circul. Res., 108(1):113-128. [doi:10.1161/CIRCRESAHA.110.223610]
51. Trayanova, N.A., Constantino, J., Gurev, V., 2011. Electromechanical models of the ventricles. Am. J. Physiol. Heart Circ. Physiol., 301(2):H279-H286. [doi:10.1152/ajpheart.00324.2011]
52. Usyk, T.P., McCulloch, A.D., 2003a. Electromechanical model of cardiac resynchronization in the dilated failing heart with left bundle branch block. J. Electrocardiol., 36(Suppl. 1): 57-61. [doi:10.1016/j.jelectrocard.2003.09.015] (Pubitemid 38049762)
53. Usyk, T.P., McCulloch, A.D., 2003b. Relationship between regional shortening and asynchronous electrical activation in a three-dimensional model of ventricular electromechanics. J. Cardiovasc. Electrophysiol., 14(S10): S196-S202. [doi:10.1046/j.1540.8167.90311.x] (Pubitemid 37393003)
54. Vasquez, C., Moreno, A.P., Berbari, E., 2004. Modeling fibroblast-mediated conduction in the ventricle. Computer in Cardiology 2004. p.349-352. [doi:10.1109/CIC.2004.1442944] (Pubitemid 41696135)
55. Xia, L., Huo, M., Wei, Q., et al., 2005. Analysis of cardiac ventricular wall motion based on a three-dimensional electromechanical biventricular model. Phys. Med. Biol., 50(8):1901-1917. [doi:10.1088/0031-9155/50/8/018] (Pubitemid 41223656)
56. Xia, L., Huo, M., Wei, Q., et al., 2006. Electrodynamic heart model construction and ECG simulation. Meth. Inf. Med., 45(5):564-573. (Pubitemid 44606726)
57. Xie, Y., Garfinkel, A., Weiss, J.N., et al., 2009a. Cardiac alternans induced by fibroblast-myocyte coupling: mechanistic insights from computational models. Am. J. Physiol. Heart Circ. Physiol., 297(2):H775-H784. [doi:10.1152/ajpheart.00341.2009]
58. Xie, Y., Garfinkel, A., Camelliti, P., et al., 2009b. Effects of fibroblast-myocyte coupling on cardiac conduction and vulnerability to reentry: a computational study. Heart Rhythm, 6(11):1641-1649. [doi:10.1016/j.hrthm.2009. 08.003]
59. Yao, J.A., Gutstein, D.E., Liu, F., et al., 2003. Cell coupling between ventricular myocyte pairs from connexin43- deficient murine hearts. Circul. Res., 93(8):736-743. [doi:10.1161/01.RES.0000095977.66660.86] (Pubitemid 37288668)
60. Zlochiver, S., Munoz, V., Vikstrom, K.L., et al., 2008. Electrotonic myofibroblast-to-myocyte coupling increases propensity to reentrant arrhythmias in two-dimensional cardiac monolayers. Biophys. J., 95(9):4469-4480. [doi:10.1529/biophysj.108.136473]