Modulation of cardiac tissue electrophysiological properties with light-sensitive proteins

Cardiovascular Research

Volumn 102, Issue 1, 2014, Pages 176-187

  Nussinovitch, Udi ^a   Shinnawi, Rami ^a   Gepstein, Lior ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Cardiac resynchronization therapy; Cell and gene therapies; Conduction block; Optogenetics; Pacing

Indexed keywords

ARCHAERHODOPSIN T; CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG; ANTIARRHYTHMIC AGENT;

ANIMAL CELL; ARTICLE; BLUE LIGHT; CELL CULTURE; COCULTURE; CONTROLLED STUDY; ELECTRIC ACTIVITY; EMBRYONIC STEM CELL; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HEART CONTRACTION; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CELL; HEART MUSCLE EXCITABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; OPTOGENETICS; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; RAT; SLOW INWARD CURRENT; ACTION POTENTIAL; ANIMAL; DRUG EFFECTS; ELECTROPHYSIOLOGY; HEART; LIGHT; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES;

ACTION POTENTIALS; ANIMALS; ANTI-ARRHYTHMIA AGENTS; CELLS, CULTURED; COCULTURE TECHNIQUES; ELECTROPHYSIOLOGICAL PHENOMENA; HEART; HUMANS; LIGHT; MICE; MYOCYTES, CARDIAC; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; RATS;

EID: 84897013419     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu037     Document Type: Article

References (39)

1. Schoenfeld MH. Contemporary pacemaker and defibrillator device therapy: challenges confronting the general cardiologist. Circulation 2007;115:638-653.
2. Cho HC, Marban E. Biological therapies for cardiac arrhythmias: can genes and cells replace drugs and devices? Circ Res 2010;106:674-685.
3. Gepstein L. Stem cells as biological heart pacemakers. Expert Opin Biol Ther 2005;5: 1531-1537.
4. Rosen MR, Robinson RB, Brink PR, Cohen IS. The road to biological pacing. Nat Rev Cardiol 2011;8:656-666.
5. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 2003;100:13940-13945.
6. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 2005;8:1263-1268.
7. Deisseroth K. Optogenetics. Nat Methods 2011;8:26-29.
8. Kravitz AV, Kreitzer AC. Optogenetic manipulation of neural circuitry in vivo. Curr Opin Neurobiol 2011;21:433-439.
9. Szobota S, Isacoff EY. Optical control of neuronal activity. Annu Rev Biophys 2010;39: 329-348.
10. Grote M, O'Malley M.A. Enlightening the life sciences: the history of halobacterial and microbial rhodopsin research. FEMS Microbiol Rev 2011;35:1082-1099.
11. Han X, Boyden ES. Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE 2007;2:e299.
12. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE, Boyden ES. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 2010;463:98-102.
13. Arrenberg AB, Stainier DY, Baier H, Huisken J. Optogenetic control of cardiac function. Science 2010;330:971-974.
14. Bruegmann T, Malan D, Hesse M, Beiert T, Fuegemann CJ, Fleischmann BK, Sasse P. Optogenetic control of heart muscle in vitro and in vivo. Nat Methods 2010;7:897-900.
15. Jia Z, Valiunas V, Lu Z, Bien H, Liu H, Wang HZ, Rosati B, Brink PR, Cohen IS, Entcheva E. Stimulating cardiac muscle by light: cardiac optogenetics by cell delivery. Circ Arrhythm Electrophysiol 2011;4:753-760.
16. Boyle PM, Williams JC, Ambrosi CM, Entcheva E, Trayanova NA. A comprehensive mul-tiscale framework for simulating optogenetics in the heart. Nat Commun 2013;4:2370.
17. Feld Y, Melamed-Frank M, Kehat I, Tal D, Marom S, Gepstein L. Electrophysiological modulation of cardiomyocytic tissue by transfected fibroblasts expressing potassium channels: a novel strategy to manipulate excitability. Circulation 2002;105:522-529.
18. Kehat I, Kenyagin-Karsenti D, Snir M, Segev H, Amit M, Gepstein A, Livne E, Binah O, Its-kovitz-Eldor J, Gepstein L. Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J Clin Invest 2001;108: 407-414.
19. Lev S, Kehat I, Gepstein L. Differentiation pathways in human embryonic stem cell-derived cardiomyocytes. Ann N Y Acad Sci 2005;1047:50-65.
20. Kehat I, Gepstein A, Spira A, Itskovitz-Eldor J, Gepstein L. High-resolution electrophysio-logical assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ Res 2002;91:659-661.
21. Chater TE, Henley JM, Brown JT, Randall AD. Voltage-and temperature-dependent gating of heterologously expressed channelrhodopsin-2. J Neurosci Methods 2010;193: 7-13.
22. Wilkoff BL, Cook JR, Epstein AE, Greene HL, Hallstrom AP, Hsia H, Kutalek SP, Sharma A. Dual-chamber pacing or ventricular backup pacing in patients with an implantable defibrillator: the Dual Chamber and VVI Implantable Defibrillator (DAVID) Trial. JAMA 2002;288:3115-3123.
23. Bristow MR, Saxon LA, Boehmer J, Krueger S, Kass DA, De Marco T, Carson P, Di Carlo L, De Mets D, White BG, De Vries DW, Feldman AM. Cardiac-resynchronization therapy with or without an implantable defibrillator in advanced chronic heart failure. N Engl J Med 2004;350:2140-2150.
24. Potapova I, Plotnikov A, Lu Z, Danilo P Jr, Valiunas V, Qu J, Doronin S, Zuckerman J, Shlapakova IN, Gao J, Pan Z, Herron AJ, Robinson RB, Brink PR, Rosen MR, Cohen IS. Human mesenchymal stem cells as a gene delivery system to create cardiac pacemakers. Circ Res 2004;94:952-959.
25. Yankelson L, Feld Y, Bressler-Stramer T, Itzhaki I, Huber I, Gepstein A, Aronson D, Marom S, Gepstein L. Cell therapy for modification of the myocardial electrophysio-logical substrate. Circulation 2008;117:720-731.
26. Hofshi A, Itzhaki I, Gepstein A, Arbel G, Gross GJ, Gepstein L. A combined gene and cell therapy approach for restoration of conduction. Heart Rhythm 2011;8:121-130.
27. Plotnikov AN, Shlapakova I, Szabolcs MJ, Danilo P Jr, Lorell BH, Potapova IA, Lu Z, Rosen AB, Mathias RT, Brink PR, Robinson RB, Cohen IS, Rosen MR. Xenografted adult human mesenchymal stem cells provide a platform for sustained biological pacemaker function in canine heart. Circulation 2007;116:706-713.
28. Fast VG, Darrow BJ, Saffitz JE, Kleber AG. Anisotropic activation spread in heart cell monolayers assessed by high-resolution optical mapping. Role of tissue discontinuities. Circ Res 1996;79:115-127.
29. 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.
30. Kizana E, Ginn SL, Smyth CM, Boyd A, Thomas SP, Allen DG, Ross DL, Alexander IE. Fibroblasts modulate cardiomyocyte excitability: implications for cardiac gene therapy. Gene Ther 2006;13:1611-1615.
31. Rook MB, Jongsma HJ, de Jonge B. Single channel currents of homo-and heterologous gap junctions between cardiac fibroblasts and myocytes. Pflugers Arch 1989;414:95-98.
32. Camelliti P, Devlin GP, Matthews KG, Kohl P, Green CR. Spatially and temporally distinct expression of fibroblast connexins after sheep ventricular infarction. Cardiovasc Res 2004;62:415-425.
33. Camelliti P, Green CR, Le Grice 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.
34. 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 1992;24:567-578.
35. Zhang Y, Kanter EM, Yamada KA. Remodeling ofcardiacfibroblasts following myocardial infarction resultsinincreased gap junction intercellular communication. Cardiovasc Pathol 2010;19:e233-e240.
36. Kehat I, Khimovich L, Caspi O, Gepstein A, Shofti R, Arbel G, Huber I, Satin J, Itskovitz-Eldor J, Gepstein L. Electromechanical integration of cardiomyocytes derived from human embryonic stem cells. Nat Biotechnol 2004;22:1282-1289.
37. Kapoor N, Liang W, Marban E, Cho HC. Direct conversionofquiescent cardiomyocytes to pacemaker cells by expression of Tbx18. Nat Biotechnol 2013;31:54-62.
38. Gepstein L, Goldin A, Lessick J, Hayam G, Shpun S, Schwartz Y, Hakim G, Shofty R, Turgeman A, Kirshenbaum D, Ben-Haim SA. Electromechanical characterization of chronic myocardial infarction in the canine coronary occlusion model. Circulation 1998;98:2055-2064.
39. Wolf T, Gepstein L, Dror U, Hayam G, Shofti R, Zaretzky A, Uretzky G, Oron U, Ben-Haim SA. Detailed endocardial mapping accurately predicts the transmural extent of myocardial infarction. J Am Coll Cardiol 2001;37:1590-1597.