Computational modeling of cardiac optogenetics: Methodology overview & review of findings from simulations

Computers in Biology and Medicine

Volumn 65, Issue , 2015, Pages 200-208

  Boyle, Patrick M ^a   Karathanos, Thomas V ^a   Entcheva, Emilia ^b   Trayanova, Natalia A ^a  

^a Johns Hopkins University   (United States)

^b St Francis Hospital The Heart Center   (United States)

Author keywords

Cardiac arrhythmia; Cardiac optogenetics; Cell delivery; Light attenuation; Multiscale computational simulations; Optical stimulation; Viral gene delivery

Indexed keywords

CELLS; CYTOLOGY; GENE EXPRESSION; GENE TRANSFER; GENES; MEDICAL COMPUTING; TISSUE;

CARDIAC ARRHYTHMIA; CELL DELIVERY; COMPUTATIONAL SIMULATION; LIGHT ATTENUATION; OPTICAL STIMULATION; OPTOGENETICS; VIRAL GENES;

HEART;

OPSIN;

ACTION POTENTIAL; ACTION POTENTIAL DURATION; ARTICLE; CARDIAC OPTOGENETICS; COMPUTER SIMULATION; DEFIBRILLATION; ELECTROSTIMULATION; HEART ARRHYTHMIA; HEART MUSCLE CELL; HEART MUSCLE CONDUCTION SYSTEM; HUMAN; ILLUMINATION; LIGHT SCATTERING; MEMBRANE CURRENT; NONHUMAN; OPTOGENETICS; PHOTOSENSITIZATION; PRIORITY JOURNAL; PURKINJE FIBER; SINUS RHYTHM; VIRAL GENE DELIVERY SYSTEM; ANIMAL; BIOLOGICAL MODEL; HEART; HEART DISEASE; PATHOPHYSIOLOGY;

ANIMALS; COMPUTER SIMULATION; HEART; HEART DISEASES; HUMANS; MODELS, CARDIOVASCULAR;

EID: 84942370059     PISSN: 00104825     EISSN: 18790534     Source Type: Journal    
DOI: 10.1016/j.compbiomed.2015.04.036     Document Type: Article

References (89)

1. Entcheva E. Cardiac optogenetics. Am. J. Physiol. Heart Circ. Physiol 2013, 304(9):H1179-H1191.
2. Boyle PM, Karathanos TV, Trayanova NA. Beauty is a Light in the Heart: The Transformative Potential of Optogenetics for Clinical Applications in Cardiovascular Medicine. Trends in Cardiovascular Medicine(0).
3. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(24):13940-13945.
4. Boyden ES, Zhang F, Bamberg E, Nagel G, Millisecond-timescale Deisseroth K. genetically targeted optical control of neural activity. Nat. Neurosci. 2005, 8(9):1263-1268.
5. Zhang F, Wang LP, Boyden ES, Deisseroth K. Channelrhodopsin-2 and optical control of excitable cells. Nat. Methods. 2006, 3(10):785-792.
6. Han X, Boyden ES. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS One 2007, 2(3):e299.
7. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010, 463(7277):98-102.
8. Gradinaru V, Zhang F, Ramakrishnan C, Mattis J, Prakash R, Diester I, et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141(1):154-165.
9. Bruegmann T, Malan D, Hesse M, Beiert T, Fuegemann CJ, Fleischmann BK, et al. Optogenetic control of heart muscle in vitro and in vivo. Nat. Methods. 2010, 7(11):897-900.
10. Jia Z, Valiunas V, Lu Z, Bien H, Liu H, Wang HZ, et al. Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery. Circ. Arrhythm Electrophysiol 2011, 4(5):753-760.
11. Nussinovitch U, Shinnawi R, Gepstein L. Modulation of cardiac tissue electrophysiological properties with light-sensitive proteins. Cardiovasc. Res. 2014, 102(1):176-187.
12. Arrenberg AB, Stainier DY, Baier H, Huisken J. Optogenetic control of cardiac function. Science 2010, 330(6006):971-974.
13. Vogt CC, Bruegmann T, Malan D, Ottersbach A, Roell W, Fleischmann BK, et al. Systemic gene transfer enables optogenetic pacing of mouse hearts. Cardiovasc. Res. 2015, 106(2):338-343.
14. Boyle PM, Entcheva E, Trayanova NA. See the light: can optogenetics restore healthy heartbeats? And, if it can, is it really worth the effort?. Expert Rev. Cardiovasc. Ther. 2014, 12(1):17-20.
15. Ambrosi CM, Klimas A, Yu J, Entcheva E. Cardiac applications of optogenetics. Prog. Biophys. Mol. Biol. 2014, 115(2-3):294-304.
16. Rudy Y, Ackerman MJ, Bers DM, Clancy CE, Houser SR, London B, et al. Systems approach to understanding electromechanical activity in the human heart: a national heart, lung, and blood institute workshop summary. Circulation 2008, 118(11):1202-1211.
17. Trayanova NA, Rice JJ. Cardiac electromechanical models: from cell to organ. Front. Physiol 2011, 2:43.
18. Trayanova NA, O'Hara T, Bayer JD, Boyle PM, McDowell KS, Constantino J, et al. Computational cardiology: how computer simulations could be used to develop new therapies and advance existing ones. Europace 2012, 14(Suppl. 5):v82-v89.
19. Trayanova NA, Boyle PM. Advances in modeling ventricular arrhythmias: from mechanisms to the clinic. Wiley Interdiscip. Rev. Syst. Biol. Med 2014, 6(2):209-224.
20. Arevalo H, Rodriguez B, Trayanova N. Arrhythmogenesis in the heart: multiscale modeling of the effects of defibrillation shocks and the role of electrophysiological heterogeneity. Chaos 2007, 17(1):015103.
21. Moreno JD, Zhu ZI, Yang PC, Bankston JR, Jeng MT, Kang C, et al. A computational model to predict the effects of class I anti-arrhythmic drugs on ventricular rhythms. Sci. Transl. Med. 2011, 3(98). 98ra83.
22. McDowell KS, Arevalo HJ, Maleckar MM, Trayanova NA. Susceptibility to arrhythmia in the infarcted heart depends on myofibroblast density. Biophys. J. 2011, 101(6):1307-1315.
23. Bordas R, Gillow K, Lou Q, Efimov IR, Gavaghan D, Kohl P, et al. Rabbit-specific ventricular model of cardiac electrophysiological function including specialized conduction system. Prog. Biophys. Mol. Biol. 2011, 107(1):90-100.
24. Boyle PM, Veenhuyzen GD, Vigmond EJ. Fusion during entrainment of orthodromic reciprocating tachycardia is enhanced for basal pacing sites but diminished when pacing near Purkinje system end points. Heart Rhythm. 2013, 10(3):444-451.
25. Boyle PM, Masse S, Nanthakumar K, Vigmond EJ. Transmural IK(ATP) heterogeneity as a determinant of activation rate gradient during early ventricular fibrillation: mechanistic insights from rabbit ventricular models. Heart Rhythm. 2013, 10(11):1710-1717.
26. Deo M, Ruan Y, Pandit SV, Shah K, Berenfeld O, Blaufox A, et al. KCNJ2 mutation in short QT syndrome 3 results in atrial fibrillation and ventricular proarrhythmia. Proc. Natl. Acad. Sci. U.S.A. 2013, 110(11):4291-4296.
27. Boyle PM, Park CJ, Arevalo HJ, Vigmond EJ, Trayanova NA. Sodium current reduction unmasks a structure-dependent substrate for arrhythmogenesis in the normal ventricles. PLoS One 2014, 9(1):e86947.
28. Chang KC, Bayer JD, Trayanova NA. Disrupted calcium release as a mechanism for atrial alternans associated with human atrial fibrillation. PLoS Comput. Biol. 2014, 10(12):e1004011.
29. Sadrieh A, Domanski L, Pitt-Francis J, Mann SA, Hodkinson EC, Ng CA, et al. Multiscale cardiac modelling reveals the origins of notched T waves in long QT syndrome type 2. Nat. Commun 2014, 5:5069.
30. Niederer SA, Smith NP. 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. 2009, 5(4):e1000371.
31. Gurev V, Constantino J, Rice JJ, Trayanova NA. Distribution of electromechanical delay in the heart: insights from a three-dimensional electromechanical model. Biophys. J. 2010, 99(3):745-754.
32. Hu Y, Gurev V, Constantino J, Trayanova N. Efficient preloading of the ventricles by a properly timed atrial contraction underlies stroke work improvement in the acute response to cardiac resynchronization therapy. Heart Rhythm. 2013, 10(12):1800-1806.
33. Hu Y, Gurev V, Constantino J, Trayanova N. Optimizing cardiac resynchronization therapy to minimize ATP consumption heterogeneity throughout the left ventricle: a simulation analysis using a canine heart failure model. Heart Rhythm. 2014, 11(6):1063-1069.
34. Tandri H, Weinberg SH, Chang KC, Zhu R, Trayanova NA, Tung L, et al. Reversible cardiac conduction block and defibrillation with high-frequency electric field. Sci. Transl. Med. 2011, 3(102). 102ra96.
35. Rantner LJ, Tice BM, Trayanova NA. Terminating ventricular tachyarrhythmias using far-field low-voltage stimuli: mechanisms and delivery protocols. Heart Rhythm. 2013, 10(8):1209-1217.
36. Rantner LJ, Vadakkumpadan F, Spevak PJ, Crosson JE, Trayanova NA. Placement of implantable cardioverter-defibrillators in paediatric and congenital heart defect patients: a pipeline for model generation and simulation prediction of optimal configurations. J. Physiol. 2013, 591(Pt 17):4321-4334.
37. Vadakkumpadan F, Rantner LJ, Tice B, Boyle P, Prassl AJ, Vigmond E, et al. Image-based models of cardiac structure with applications in arrhythmia and defibrillation studies. J. Electrocardiol. 2009, 42(2):157 e1-10.
38. Lamata P, Niederer S, Nordsletten D, Barber DC, Roy I, Hose DR, et al. An accurate, fast and robust method to generate patient-specific cubic Hermite meshes. Med. Image Anal. 2011, 15(6):801-813.
39. Niederer SA, Plank G, Chinchapatnam P, Ginks M, Lamata P, Rhode KS, et al. Length-dependent tension in the failing heart and the efficacy of cardiac resynchronization therapy. Cardiovasc. Res. 2011, 89(2):336-343.
40. Ashikaga H, Arevalo H, Vadakkumpadan F, Blake RC, Bayer JD, Nazarian S, et al. Feasibility of image-based simulation to estimate ablation target in human ventricular arrhythmia. Heart Rhythm. 2013, 10(8):1109-1116.
41. Arevalo H, Plank G, Helm P, Halperin H, Trayanova N. Tachycardia in post-infarction hearts: insights from 3D image-based ventricular models. PLoS One 2013, 8(7):e68872.
42. Vadakkumpadan F, Trayanova N, Wu KC. Image-based left ventricular shape analysis for sudden cardiac death risk stratification. Heart Rhythm. 2014, 11(10):1693-1700.
43. Prakosa A, Malamas P, Zhang S, Pashakhanloo F, Arevalo H, Herzka DA, et al. Methodology for image-based reconstruction of ventricular geometry for patient-specific modeling of cardiac electrophysiology. Prog. Biophys. Mol. Biol. 2014, 115(2-3):226-234.
44. Boyle PM, Williams JC, Ambrosi CM, Entcheva E, Trayanova NA. A comprehensive multiscale framework for simulating optogenetics in the heart. Nat. Commun 2013, 4:2370.
45. Bamann C, Kirsch T, Nagel G, Bamberg E. Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. J. Mol. Biol. 2008, 375(3):686-694.
46. Hegemann P, Ehlenbeck S, Gradmann D. Multiple photocycles of channelrhodopsin. Biophys. J. 2005, 89(6):3911-3918.
47. Nikolic K, Grossman N, Grubb MS, Burrone J, Toumazou C, Degenaar P. Photocycles of channelrhodopsin-2. Photochem. Photobiol. 2009, 85(1):400-411.
48. Williams JC, Xu J, Lu Z, Klimas A, Chen X, Ambrosi CM, et al. Computational optogenetics: empirically-derived voltage- and light-sensitive channelrhodopsin-2 model. PLoS Comput. Biol. 2013, 9(9). e1003220-e.
49. Entcheva E, Williams JC. Channelrhodopsin2 current during the action potential: optical AP clamp and approximation. Sci. Rep 2014, 4:5838.
50. ten Tusscher KHWJ Panfilov AV. Alternans and spiral breakup in a human ventricular tissue model. Am. J. Physiol. Heart Circ. Physiol 2006, 291(3):H1088-H1100.
51. Park SA, Lee SR, Tung L, Yue DT. Optical mapping of optogenetically shaped cardiac action potentials. Sci. Rep 2014, 4:6125.
52. Nikolic K, Jarvis S, Grossman N, Schultz S. Computational models of optogenetic tools for controlling neural circuits with light. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2013;2013:5934-5937.
53. Chow BY, Han X, Boyden ES. Genetically encoded molecular tools for light-driven silencing of targeted neurons. Prog. Brain Res. 2012, 196:49-61.
54. Kleinlogel S, Feldbauer K, Dempski RE, Fotis H, Wood PG, Bamann C, et al. Ultra light-sensitive and fast neuronal activation with the Ca(2)+-permeable channelrhodopsin CatCh. Nat. Neurosci. 2011, 14(4):513-518.
55. Bingen BO, Engels MC, Schalij MJ, Jangsangthong W, Neshati Z, Feola I, et al. Light-induced termination of spiral wave arrhythmias by optogenetic engineering of atrial cardiomyocytes. Cardiovasc. Res. 2014, 104(1):194-205.
56. Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, et al. Independent optical excitation of distinct neural populations. Nat. Methods. 2014, 11(3):338-346.
57. Lin JY, Knutsen PM, Muller A, Kleinfeld D, Tsien RY. ReaChR: a red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat. Neurosci. 2013, 16(10):1499-1508.
58. Williams JC, Xu J, Lu Z, Klimas A, Chen X, Ambrosi CM, et al. Computational optogenetics: empirically-derived voltage- and light-sensitive channelrhodopsin-2 model. PLoS Comput. Biol. 2013, 9(9):e1003220.
59. Ambrosi CM, Entcheva E. Optogenetic control of cardiomyocytes via viral delivery. Methods Mol. Biol. 2014, 1181:215-228.
60. Hofmann B, Maybeck V, Eick S, Meffert S, Ingebrandt S, Wood P, et al. Light induced stimulation and delay of cardiac activity. Lab. Chip. 2010, 10(19):2588-2596.
61. Abilez OJ, Wong J, Prakash R, Deisseroth K, Zarins CK, Kuhl E. Multiscale computational models for optogenetic control of cardiac function. Biophys. J. 2011, 101(6):1326-1334.
62. Beiert T, Bruegmann T, Sasse P. Optogenetic activation of Gq signalling modulates pacemaker activity of cardiomyocytes. Cardiovasc. Res. 2014, 102(3):507-516.
63. Ambrosi CM, Klimas A, Yu J, Entcheva E. Cardiac applications of optogenetics. Prog. Biophys. Mol. Biol. 2014.
64. Rosen AB, Kelly DJ, Schuldt AJT, Lu J, Potapova IA, Doronin SV, et al. Finding fluorescent needles in the cardiac haystack: tracking human mesenchymal stem cells labeled with quantum dots for quantitative in vivo three-dimensional fluorescence analysis. Stem Cells. 2007, 25(8):2128-2138.
65. Prasad K-MR, Smith RS, Xu Y, French BA. A single direct injection into the left ventricular wall of an adeno-associated virus 9 (AAV9) vector expressing extracellular superoxide dismutase from the cardiac troponin-T promoter protects mice against myocardial infarction. J. Gene Med. 2011, 13(6):333-341.
66. Prasad KM, Xu Y, Yang Z, Acton ST, French BA. Robust cardiomyocyte-specific gene expression following systemic injection of AAV: in vivo gene delivery follows a Poisson distribution. Gene Ther 2011, 18(1):43-52.
67. Comtois P, Nattel S. Interactions between cardiac fibrosis spatial pattern and ionic remodeling on electrical wave propagation. in: 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Embc) 2011, 2011:4669-4672.
68. McDowell KS, Vadakkumpadan F, Blake R, Blauer J, Plank G, Macleod RS, et al. Methodology for patient-specific modeling of atrial fibrosis as a substrate for atrial fibrillation. J. Electrocardiol. 2012.
69. McDowell KS, Vadakkumpadan F, Blake R, Blauer J, Plank G, Macleod RS, et al. Mechanistic inquiry into the role of tissue remodeling in fibrotic lesions in human atrial fibrillation. Biophys. J. 2013, 104(12):2764-2773.
70. Moran PA. Notes on continuous stochastic phenomena. Biometrika 1950, 37(1-2):17-23.
71. Trayanova NA. Mathematical approaches to understanding and imaging atrial fibrillation: significance for mechanisms and management. Circ. Res. 2014, 114(9):1516-1531.
72. Trayanova NA. Whole-heart modeling: applications to cardiac electrophysiology and electromechanics. Circ Res. 2011, 108(1):113-128.
73. Klimas A, Entcheva E. Toward microendoscopy-inspired cardiac optogenetics in vivo: technical overview and perspective. J. Biomed. Opt. 2014, 19(8):080701.
74. Kim TI, McCall JG, Jung YH, Huang X, Siuda ER, Li Y, et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 2013, 340(6129):211-216.
75. Xu L, Gutbrod SR, Bonifas AP, Su Y, Sulkin MS, Lu N, et al. 3D multifunctional integumentary membranes for spatiotemporal cardiac measurements and stimulation across the entire epicardium. Nat. Commun 2014, 5:3329.
76. Baxter WT, Mironov SF, Zaitsev AV, Jalife J, Pertsov AM. Visualizing excitation waves inside cardiac muscle using transillumination. Biophys. J. 2001, 80(1):516-530.
77. Weissleder R, Ntziachristos V. Shedding light onto live molecular targets. Nat. Med 2003, 9(1):123-128.
78. Bishop MJ, Rodriguez B, Eason J, Whiteley JP, Trayanova N, Gavaghan DJ. Synthesis of voltage-sensitive optical signals: application to panoramic optical mapping. Biophys. J. 2006, 90(8):2938-2945.
79. Bishop MJ, Plank G. Simulating photon scattering effects in structurally detailed ventricular models using a Monte Carlo approach. Front. Physiol. 2014, 5.
80. Ding L, Splinter R, Knisley SB. Quantifying spatial localization of optical mapping using Monte Carlo simulations. IEEE Trans. Biomed Eng. 2001, 48(10):1098-1107.
81. Courtemanche M, Ramirez RJ, Nattel S. Ionic mechanisms underlying human atrial action potential properties: insights from a mathematical model. Am. J. Physiol. 1998, 275(1 Pt 2):301-321.
82. Sampson KJ, Iyer V, Marks AR, Kass RS. A computational model of Purkinje fibre single cell electrophysiology: implications for the long QT syndrome. J. Physiol. 2010, 588(Pt 14):2643-2655.
83. Williams John C., Entcheva Emilia Optogenetic versus electrical stimulation of human cardiomyocytes: Modeling insights. Biophys. J. 2015, 108(8):1934-1945.
84. Boyle PM, Deo M, Plank G, Vigmond EJ. Purkinje-mediated effects in the response of quiescent ventricles to defibrillation shocks. Ann. Biomed. Eng. 2010, 38(2):456-468.
85. Wong J, Abilez OJ, Kuhl E. Computational optogenetics: a novel continuum framework for the photoelectrochemistry of living systems. J. Mech. Phys. Solids. 2012, 60(6):1158-1178.
86. Provost J, Gurev V, Trayanova N, Konofagou EE. Mapping of cardiac electrical activation with electromechanical wave imaging: an in silico-in vivo reciprocity study. Heart Rhythm. 2011, 8(5):752-759.
87. Gurev V, Lee T, Constantino J, Arevalo H, Trayanova NA. Models of cardiac electromechanics based on individual hearts imaging data: image-based electromechanical models of the heart. Biomech. Model Mechanobiol. 2011, 10(3):295-306.
88. Karathanos Thomas V., Boyle Patrick M., Trayanova Natalia A. Optogenetics-enabled dynamic modulation of action potential duration in atrial tissue: feasibility of a novel therapeutic approach. Europace 2014, 16(suppl 4):iv69-iv76.
89. McDowell KS, Vadakkumpadan F, Blake R, Blauer J, Plank G, MacLeod RS, et al. Methodology for patient-specific modeling of atrial fibrosis as a substrate for atrial fibrillation. J. Electrocardiol 2012, 45(6):640-645.