A comprehensive multiscale framework for simulating optogenetics in the heart

Nature Communications

Volumn 4, Issue , 2013, Pages

  Boyle, Patrick M ^a   Williams, John C ^b   Ambrosi, Christina M ^b   Entcheva, Emilia ^b   Trayanova, Natalia A ^a  

^a Johns Hopkins University   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OPSIN;

GENETICS; NUMERICAL MODEL; PROTEIN; SPATIAL DISTRIBUTION; SPATIOTEMPORAL ANALYSIS; THRESHOLD;

ARTICLE; BEHAVIOR; CARDIAC OPTOGENETICS; CELL MEMBRANE; ELECTROSTIMULATION; ENERGY; EXCITATION; GEOMETRY; HEART ELECTROPHYSIOLOGY; HEART FUNCTION; HEART HEMODYNAMICS; HUMAN; ILLUMINATION; LIGHT; OPTOGENETICS; SENSITIVITY ANALYSIS;

CARDIAC ELECTROPHYSIOLOGY; CELL LINE; ELECTRIC STIMULATION; HEART; HUMANS; LIGHT; MYOCARDIUM; OPTOGENETICS; PHOTIC STIMULATION; RHODOPSIN;

EID: 84883437134     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3370     Document Type: Article

References (59)

1. Binggeli, C. et al. Autonomic nervous system-controlled cardiac pacing: a comparison between intracardiac impedance signal and muscle sympathetic nerve activity. Pacing Clin. Electrophysiol. 23, 1632-1637 (2000).
2. Merrill, D. R., Bikson, M. & Jefferys, J. G. R. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J. Neurosci. Methods 141, 171-198 (2005). (Pubitemid 40136531)
3. Raad, D. et al. Implantable electrophysiologic cardiac device infections: a risk factor analysis. Eur. J. Clin. Microbiol. Infect. Dis. 31, 3015-3021 (2012).
4. Kutarski, A., Pietura, R. & Czajkowski, M. Difficult dual stage transcutaneous lead extraction complicated by fracture of both leads. Cardiol. J. 19, 412-417 (2012).
5. Brenyo, A., Goldenberg, I. & Barsheshet, A. The downside of right ventricular apical pacing. Indian Pacing Electrophysiol. J. 12, 102-113 (2012).
6. Andersen, H. R. et al. Long-term follow-up of patients from a randomised trial of atrial versus ventricular pacing for sick-sinus syndrome. Lancet 350, 1210-1216 (1997). (Pubitemid 127445094)
7. Al-Khadra, A., Nikolski, V. & Efimov, I. R. The role of electroporation in defibrillation. Circ. Res. 87, 797-804 (2000).
8. Eysmann, S. B., Marchlinski, F. E., Buxton, A. E. & Josephson, M. E. Electrocardiographic changes after cardioversion of ventricular arrhythmias. Circulation 73, 73-81 (1986). (Pubitemid 16132414)
9. Mollerus, M. & Naslund, L. Myocardial stunning following defibrillation threshold testing. J. Interv. Card. Electrophysiol. 19, 213-216 (2007). (Pubitemid 47573211)
10. Moss, A. J. et al. Prophylactic implantation of a defibrillator in patients with myocardial infarction and reduced ejection fraction. N Engl J Med 346, 877-883 (2002). (Pubitemid 34984635)
11. Larsen, G. K., Evans, J., Lambert, W. E., Chen, Y. & Raitt, M. H. Shocks burden and increased mortality in implantable cardioverter-defibrillator patients. Heart Rhythm 8, 1881-1886 (2011).
12. Maisel, W. H. Pacemaker and icd generator reliability: meta-analysis of device registries. JAMA 295, 1929-1934 (2006).
13. Marcus, G. M., Chan, D. W. & Redberg, R. F. Recollection of pain due to inappropriate versus appropriate implantable cardioverter-defibrillator shocks. Pacing. Clin. Electrophysiol. 34, 348-353 (2011).
14. Boodhoo, L. et al. The safety and effectiveness of a nurse led cardioversion service under sedation. Heart 90, 1443-1446 (2004). (Pubitemid 39626322)
15. Deisseroth, K. Optogenetics. Nat. Methods 8, 26-29 (2011).
16. Tsubota, T., Ohashi, Y., Tamura, K., Sato, A. & Miyashita, Y. Optogenetic manipulation of cerebellar Purkinje cell activity in vivo. PLoS One 6, e22400 (2011).
17. Gradinaru, V. et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 141, 154-165 (2010).
18. Arrenberg, A. B., Stainier, D. Y. R., Baier, H. & Huisken, J. Optogenetic control of cardiac function. Science 330, 971-974 (2010).
19. Entcheva, E. Cardiac optogenetics. Am. J. Physiol. Heart Circ. Physiol. 304, H1179-H1191 (2013).
20. Abilez, O. J. et al. Multiscale computational models for optogenetic control of cardiac function. Biophys. J. 101, 1326-1334 (2011).
21. Jia, Z. et al. Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery. Circ. Arrhythm. Electrophysiol. 4, 753-760 (2011).
22. Bruegmann, T. et al. Optogenetic control of heart muscle in vitro and in vivo. Nat. Methods 7, 897-900 (2010).
23. Trayanova, N. A. Whole-heart modeling: applications to cardiac electrophysiology and electromechanics. Circ. Res. 108, 113-128 (2011).
24. Moreno, J. D. et al. A computational model to predict the effects of class I antiarrhythmic drugs on ventricular rhythms. Sci. Transl. Med. 3, 98ra83 (2011).
25. Boyle, P. M., Deo, M., Plank, G. & Vigmond, E. J. Purkinje-mediated effects in the response of quiescent ventricles to defibrillation shocks. Ann. Biomed. Eng. 38, 456-468 (2010).
26. Niederer, S. A. et al. Biophysical modeling to simulate the response to multisite left ventricular stimulation using a quadripolar pacing lead. Pacing Clin. Electrophysiol. 35, 204-214 (2012).
27. Bishop, M. J. et al. Development of an anatomically detailed MRI-derived rabbit ventricular model and assessment of its impact on simulations of electrophysiological function. Am. J. Physiol. Heart Circ. Physiol. 298, H699-H718 (2010).
28. ten Tusscher, K. H. W. J., Hren, R. & Panfilov, A. V. Organization of ventricular fibrillation in the human heart. Circ. Res. 100, e87-101 (2007).
29. Nikolic, K. et al. Photocycles of channelrhodopsin-2. Photochem. Photobiol. 85, 400-411 (2009).
30. Hegemann, P., Ehlenbeck, S. & Gradmann, D. Multiple photocycles of channelrhodopsin. Biophys. J. 89, 3911-3918 (2005). (Pubitemid 41725613)
31. ten Tusscher, K. H. W. J. & Panfilov, A. V. Alternans and spiral breakup in a human ventricular tissue model. Am. J. Physiol. Heart Circ. Physiol. 291, H1088-H1100 (2006). (Pubitemid 44343652)
32. Vigmond, E. J., Aguel, F. & Trayanova, N. A. Computational techniques for solving the bidomain equations in three dimensions. IEEE Trans. Biomed. Eng. 49, 1260-1269 (2002). (Pubitemid 35304164)
33. Vigmond, E. J., dos Santos, R. W., Prassl, A. J., Deo, M. & Plank, G. Solvers for the cardiac bidomain equations. Prog. Biophys. Mol. Biol. 96, 3-18 (2008). (Pubitemid 351625294)
34. Prasad, K.-M. R., Smith, R. S., Xu, Y. & French, B. A. 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. 13, 333-341 (2011).
35. Rosen, A. B. 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 25, 2128-2138 (2007). (Pubitemid 47258192)
36. Comtois, P. & Nattel, S. Interactions between cardiac fibrosis spatial pattern and ionic remodeling on electrical wave propagation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011, 4669-4672 (2011).
37. Weissleder, R. & Ntziachristos, V. Shedding light onto live molecular targets. Nat. Med. 9, 123-128 (2003). (Pubitemid 36098273)
38. Rickgauer, J. P. & Tank, D. W. Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl Acad. Sci. USA 106, 15025-15030 (2009).
39. Bishop, M. J. et al. Synthesis of voltage-sensitive optical signals: application to panoramic optical mapping. Biophys. J. 90, 2938-2945 (2006).
40. Stewart, P. et al. Mathematical models of the electrical action potential of Purkinje fibre cells. Philos. Transact. A Math. Phys. Eng. Sci. 367, 2225-2255 (2009).
41. Vigmond, E. J. & Clements, C. Construction of a computer model to investigate sawtooth effects in the Purkinje system. IEEE Trans. Biomed. Eng. 54, 389-399 (2007). (Pubitemid 46371249)
42. Waehler, R., Russell, S. J. & Curiel, D. T. Engineering targeted viral vectors for gene therapy. Nat. Rev. Genet. 8, 573-587 (2007). (Pubitemid 47077278)
43. Provost, J., Gurev, V., Trayanova, N. & Konofagou, E. E. Mapping of cardiac electrical activation with electromechanical wave imaging: an in silico-in vivo reciprocity study. Heart Rhythm 8, 752-759 (2011).
44. Gurev, V., Lee, T., Constantino, J., Arevalo, H. & Trayanova, N. A. Models of cardiac electromechanics based on individual hearts imaging data: image-based electromechanical models of the heart. Biomech. Model Mechanobiol. 10, 295-306 (2011).
45. Xie, Y., Sato, D., Garfinkel, A., Qu, Z. & Weiss, J. N. So little source, so much sink: requirements for afterdepolarizations to propagate in tissue. Biophys. J. 99, 1408-1415 (2010).
46. Barba-Pichardo, R. et al. Ventricular resynchronization therapy by direct Hisbundle pacing using an internal cardioverter defibrillator. Europace 15, 83-88 (2013).
47. Salama, G., Kanai, A. & Efimov, I. R. Subthreshold stimulation of Purkinje fibers interrupts ventricular tachycardia in intact hearts. Experimental study with voltage-sensitive dyes and imaging techniques. Circ. Res. 74, 604-619 (1994). (Pubitemid 24088521)
48. Boyle, P. M. & Vigmond, E. J. An intuitive safety factor for cardiac propagation. Biophys. J. 98, L57-L59 (2010).
49. Shimizu, W. & Antzelevitch, C. Sodium channel block with mexiletine is effective in reducing dispersion of repolarization and preventing torsade des pointes in LQT2 and LQT3 models of the long-QT syndrome. Circulation 96, 2038-2047 (1997). (Pubitemid 27400769)
50. Extramiana, F. & Antzelevitch, C. Amplified transmural dispersion of repolarization as the basis for arrhythmogenesis in a canine ventricular-wedge model of short-QT syndrome. Circulation 110, 3661-3666 (2004). (Pubitemid 39665254)
51. Glukhov, A. V. et al. Transmural dispersion of repolarization in failing and nonfailing human ventricle. Circ. Res. 106, 981-991 (2010).
52. Opthof, T. et al. The association of abnormal ventricular wall motion and increased dispersion of repolarization in humans is independent of the presence of myocardial infarction. Front. Physiol. 3, 235 (2012).
53. Talathi, S. S., Carney, P. R. & Khargonekar, P. P. Control of neural synchrony using channelrhodopsin-2: a computational study. J. Comput. Neurosci. 31, 87-103 (2011).
54. Grossman, N., Nikolic, K., Toumazou, C. & Degenaar, P. Modeling study of the light stimulation of a neuron cell with channelrhodopsin-2 mutants. IEEE Trans. Biomed. Eng. 58, 1742-1751 (2011).
55. Zimmermann, D. et al. Biophysical characterisation of electrofused giant HEK293-cells as a novel electrophysiological expression system. Biochem. Biophys. Res. Commun. 348, 673-681 (2006). (Pubitemid 44188617)
56. Vigmond, E. J., Hughes, M., Plank, G. & Leon, L. J. Computational tools for modeling electrical activity in cardiac tissue. J. Electrocardiol. 36 Suppl 69-74 (2003). (Pubitemid 38049764)
57. Mahajan, A. et al. A rabbit ventricular action potential model replicating cardiac dynamics at rapid heart rates. Biophys. J. 94, 392-410 (2008).
58. Aslanidi, O. V., Sleiman, R. N., Boyett, M. R., Hancox, J. C. & Zhang, H. Ionic mechanisms for electrical heterogeneity between rabbit Purkinje fiber and ventricular cells. Biophys. J. 98, 2420-2431 (2010).
59. Boyle, P. M., Veenhuyzen, G. D. & Vigmond, E. J. Fusion during entrainment of orthodromic reciprocating tachycardia is enhanced for basal pacing sites but diminished when pacing near Purkinje system end points. Heart Rhythm 10, 444-451 (2013